diff --git a/cmd/generate-config/config/config-openapi-spec.json b/cmd/generate-config/config/config-openapi-spec.json
index 901548610d..4d5d03a2db 100755
--- a/cmd/generate-config/config/config-openapi-spec.json
+++ b/cmd/generate-config/config/config-openapi-spec.json
@@ -245,6 +245,11 @@
           "default": "example.com",
           "example": "microshift.example.com"
         },
+        "configFile": {
+          "description": "configFile is the path to a custom CoreDNS Corefile on the host filesystem.\nWhen set, MicroShift uses this file as the Corefile in the dns-default ConfigMap,\nfully replacing the default template-rendered configuration.\nChanges to this file are detected at runtime and applied without restarting MicroShift.\nMutually exclusive with dns.hosts: setting both causes a startup error.",
+          "type": "string",
+          "example": "/etc/microshift/dns/Corefile"
+        },
         "hosts": {
           "description": "Hosts contains configuration for the hosts file.",
           "type": "object",
diff --git a/docs/user/howto_config.md b/docs/user/howto_config.md
index cbed9baa28..72cd84df6e 100644
--- a/docs/user/howto_config.md
+++ b/docs/user/howto_config.md
@@ -40,6 +40,7 @@ debugging:
     logLevel: ""
 dns:
     baseDomain: ""
+    configFile: ""
     hosts:
         file: ""
         status: ""
@@ -198,6 +199,7 @@ debugging:
     logLevel: Normal
 dns:
     baseDomain: example.com
+    configFile: ""
     hosts:
         file: /etc/hosts
         status: Disabled
diff --git a/packaging/microshift/config.yaml b/packaging/microshift/config.yaml
index fd45f1a37a..7d54331024 100644
--- a/packaging/microshift/config.yaml
+++ b/packaging/microshift/config.yaml
@@ -72,6 +72,14 @@ dns:
     # example:
     #   microshift.example.com
     baseDomain: example.com
+    # configFile is the path to a custom CoreDNS Corefile on the host filesystem.
+    # When set, MicroShift uses this file as the Corefile in the dns-default ConfigMap,
+    # fully replacing the default template-rendered configuration.
+    # Changes to this file are detected at runtime and applied without restarting MicroShift.
+    # Mutually exclusive with dns.hosts: setting both causes a startup error.
+    # example:
+    #   /etc/microshift/dns/Corefile
+    configFile: ""
     # Hosts contains configuration for the hosts file.
     hosts:
         # File is the path to the hosts file to monitor.
diff --git a/pkg/cmd/run.go b/pkg/cmd/run.go
index bd32bb8782..d8dff2a4f4 100644
--- a/pkg/cmd/run.go
+++ b/pkg/cmd/run.go
@@ -236,6 +236,7 @@ func RunMicroshift(cfg *config.Config) error {
 	util.Must(m.AddService(controllers.NewClusterID(cfg)))
 	util.Must(m.AddService(controllers.NewTelemetryManager(cfg)))
 	util.Must(m.AddService(controllers.NewHostsWatcherManager(cfg)))
+	util.Must(m.AddService(controllers.NewDNSConfigurationWatcherManager(cfg)))
 	util.Must(m.AddService(gdp.NewGenericDevicePlugin(cfg)))
 
 	// Storing and clearing the env, so other components don't send the READY=1 until MicroShift is fully ready
diff --git a/pkg/components/controllers.go b/pkg/components/controllers.go
index e9bdf7af50..ded367dfca 100644
--- a/pkg/components/controllers.go
+++ b/pkg/components/controllers.go
@@ -291,10 +291,9 @@ func startDNSController(ctx context.Context, cfg *config.Config, kubeconfigPath
 			"components/openshift-dns/dns/service-account.yaml",
 			"components/openshift-dns/node-resolver/service-account.yaml",
 		}
-		cm = []string{
-			"components/openshift-dns/dns/configmap.yaml",
-		}
-		svc = []string{
+		cm     = "components/openshift-dns/dns/configmap.yaml"
+		cmList = []string{cm}
+		svc    = []string{
 			"components/openshift-dns/dns/service.yaml",
 		}
 	)
@@ -303,9 +302,10 @@ func startDNSController(ctx context.Context, cfg *config.Config, kubeconfigPath
 		return err
 	}
 
+	hostsEnabled := cfg.DNS.Hosts.Status == config.HostsStatusEnabled
 	extraParams := assets.RenderParams{
 		"ClusterIP":    cfg.Network.DNS,
-		"HostsEnabled": cfg.DNS.Hosts.Status == config.HostsStatusEnabled,
+		"HostsEnabled": hostsEnabled,
 	}
 
 	if err := assets.ApplyServices(ctx, svc, renderTemplate, renderParamsFromConfig(cfg, extraParams), kubeconfigPath); err != nil {
@@ -333,10 +333,24 @@ func startDNSController(ctx context.Context, cfg *config.Config, kubeconfigPath
 		klog.Warningf("Failed to apply serviceAccount %v %v", sa, err)
 		return err
 	}
-	if err := assets.ApplyConfigMaps(ctx, cm, renderTemplate, renderParamsFromConfig(cfg, extraParams), kubeconfigPath); err != nil {
-		klog.Warningf("Failed to apply configMap %v %v", cm, err)
-		return err
+
+	if cfg.DNS.ConfigFile != "" {
+		corefileContent, err := os.ReadFile(cfg.DNS.ConfigFile)
+		if err != nil {
+			klog.Warningf("Failed to read custom DNS config file %s: %v", cfg.DNS.ConfigFile, err)
+			return err
+		}
+		if err := assets.ApplyConfigMapWithData(ctx, cm, map[string]string{"Corefile": string(corefileContent)}, kubeconfigPath); err != nil {
+			klog.Warningf("Failed to apply custom DNS configMap: %v", err)
+			return err
+		}
+	} else {
+		if err := assets.ApplyConfigMaps(ctx, cmList, renderTemplate, renderParamsFromConfig(cfg, extraParams), kubeconfigPath); err != nil {
+			klog.Warningf("Failed to apply configMap %v %v", cmList, err)
+			return err
+		}
 	}
+
 	if err := assets.ApplyDaemonSets(ctx, apps, renderTemplate, renderParamsFromConfig(cfg, extraParams), kubeconfigPath); err != nil {
 		klog.Warningf("Failed to apply apps %v %v", apps, err)
 		return err
diff --git a/pkg/config/config.go b/pkg/config/config.go
index cffb723f2c..192ee26d73 100644
--- a/pkg/config/config.go
+++ b/pkg/config/config.go
@@ -212,6 +212,9 @@ func (c *Config) incorporateUserSettings(u *Config) {
 	if u.DNS.BaseDomain != "" {
 		c.DNS.BaseDomain = u.DNS.BaseDomain
 	}
+	if u.DNS.ConfigFile != "" {
+		c.DNS.ConfigFile = u.DNS.ConfigFile
+	}
 
 	if u.Network.CNIPlugin != "" {
 		c.Network.CNIPlugin = u.Network.CNIPlugin
diff --git a/pkg/config/dns.go b/pkg/config/dns.go
index d8948449c9..b567cbbc08 100644
--- a/pkg/config/dns.go
+++ b/pkg/config/dns.go
@@ -27,6 +27,15 @@ type DNS struct {
 	// +kubebuilder:example=microshift.example.com
 	BaseDomain string `json:"baseDomain"`
 
+	// configFile is the path to a custom CoreDNS Corefile on the host filesystem.
+	// When set, MicroShift uses this file as the Corefile in the dns-default ConfigMap,
+	// fully replacing the default template-rendered configuration.
+	// Changes to this file are detected at runtime and applied without restarting MicroShift.
+	// Mutually exclusive with dns.hosts: setting both causes a startup error.
+	// +optional
+	// +kubebuilder:example="/etc/microshift/dns/Corefile"
+	ConfigFile string `json:"configFile,omitempty"`
+
 	// Hosts contains configuration for the hosts file.
 	Hosts HostsConfig `json:"hosts,omitempty"`
 }
@@ -59,36 +68,31 @@ func dnsDefaults() DNS {
 }
 
 func (t *DNS) validate() error {
-	switch t.Hosts.Status {
-	case HostsStatusEnabled:
-		if t.Hosts.File == "" {
-			break
-		}
+	if t.ConfigFile != "" && t.Hosts.Status == HostsStatusEnabled {
+		return fmt.Errorf("dns.configFile and dns.hosts are mutually exclusive")
+	}
 
-		cleanPath := filepath.Clean(t.Hosts.File)
+	if err := t.validateConfigFile(); err != nil {
+		return err
+	}
 
-		fi, err := os.Stat(cleanPath)
-		// Enforce ConfigMap requirement: the file must not exceed 1MiB, as it will be mounted into a ConfigMap.
-		if err == nil && fi.Size() > 1048576 {
-			return fmt.Errorf("hosts file %s exceeds 1MiB ConfigMap (and internal buffer) size limit (got %d bytes)", t.Hosts.File, fi.Size())
-		}
-		if !filepath.IsAbs(cleanPath) {
-			return fmt.Errorf("hosts file path must be absolute: got %s", t.Hosts.File)
-		}
+	return t.validateHosts()
+}
 
-		_, err = os.Stat(cleanPath)
-		if os.IsNotExist(err) {
-			return fmt.Errorf("hosts file %s does not exist", t.Hosts.File)
-		} else if err != nil {
-			return fmt.Errorf("error checking hosts file %s: %v", t.Hosts.File, err)
-		}
+func (t *DNS) validateConfigFile() error {
+	if t.ConfigFile == "" {
+		return nil
+	}
+	return validateFilePath(t.ConfigFile, "dns config file")
+}
 
-		file, err := os.Open(t.Hosts.File)
-		if err != nil {
-			return fmt.Errorf("hosts file %s is not readable: %v", t.Hosts.File, err)
+func (t *DNS) validateHosts() error {
+	switch t.Hosts.Status {
+	case HostsStatusEnabled:
+		if t.Hosts.File == "" {
+			break
 		}
-		return file.Close()
-
+		return validateFilePath(t.Hosts.File, "hosts file")
 	case HostsStatusDisabled:
 		return nil
 	default:
@@ -96,3 +100,34 @@ func (t *DNS) validate() error {
 	}
 	return nil
 }
+
+func validateFilePath(path, label string) error {
+	cleanPath := filepath.Clean(path)
+	if !filepath.IsAbs(cleanPath) {
+		return fmt.Errorf("%s path must be absolute: got %s", label, path)
+	}
+
+	fi, err := os.Stat(cleanPath)
+	if os.IsNotExist(err) {
+		return fmt.Errorf("%s %s does not exist", label, path)
+	} else if err != nil {
+		return fmt.Errorf("error checking %s %s: %v", label, path, err)
+	}
+	if !fi.Mode().IsRegular() {
+		return fmt.Errorf("%s %s must be a regular file", label, path)
+	}
+
+	if fi.Size() == 0 {
+		return fmt.Errorf("%s %s is empty", label, path)
+	}
+
+	if fi.Size() > 1048576 {
+		return fmt.Errorf("%s %s exceeds 1MiB size limit (got %d bytes)", label, path, fi.Size())
+	}
+
+	file, err := os.Open(cleanPath)
+	if err != nil {
+		return fmt.Errorf("%s %s is not readable: %v", label, path, err)
+	}
+	return file.Close()
+}
diff --git a/pkg/config/dns_test.go b/pkg/config/dns_test.go
new file mode 100644
index 0000000000..b3c21e63e1
--- /dev/null
+++ b/pkg/config/dns_test.go
@@ -0,0 +1,141 @@
+package config
+
+import (
+	"fmt"
+	"os"
+	"path/filepath"
+	"testing"
+
+	"github.com/stretchr/testify/assert"
+	"github.com/stretchr/testify/require"
+)
+
+func TestDNS_ValidateConfigFile_MutualExclusivity(t *testing.T) {
+	tmpFile := createTempCorefile(t, ".:5353 { whoami }")
+
+	dns := DNS{
+		ConfigFile: tmpFile,
+		Hosts: HostsConfig{
+			Status: HostsStatusEnabled,
+			File:   "/etc/hosts",
+		},
+	}
+	err := dns.validate()
+	assert.ErrorContains(t, err, "dns.configFile and dns.hosts are mutually exclusive")
+}
+
+func TestDNS_ValidateConfigFile_WithHostsDisabled(t *testing.T) {
+	tmpFile := createTempCorefile(t, ".:5353 { whoami }")
+
+	dns := DNS{
+		ConfigFile: tmpFile,
+		Hosts: HostsConfig{
+			Status: HostsStatusDisabled,
+		},
+	}
+	assert.NoError(t, dns.validate())
+}
+
+func TestDNS_ValidateConfigFile_EmptyConfigFilePreservesDefault(t *testing.T) {
+	dns := DNS{
+		ConfigFile: "",
+		Hosts: HostsConfig{
+			Status: HostsStatusDisabled,
+		},
+	}
+	assert.NoError(t, dns.validate())
+}
+
+func TestDNS_ValidateConfigFile_NonAbsolutePath(t *testing.T) {
+	dns := DNS{
+		ConfigFile: "relative/path/Corefile",
+		Hosts: HostsConfig{
+			Status: HostsStatusDisabled,
+		},
+	}
+	err := dns.validate()
+	assert.ErrorContains(t, err, "dns config file path must be absolute")
+}
+
+func TestDNS_ValidateConfigFile_NonExistentFile(t *testing.T) {
+	dns := DNS{
+		ConfigFile: "/tmp/nonexistent-corefile-test-12345",
+		Hosts: HostsConfig{
+			Status: HostsStatusDisabled,
+		},
+	}
+	err := dns.validate()
+	assert.ErrorContains(t, err, "does not exist")
+}
+
+func TestDNS_ValidateConfigFile_Directory(t *testing.T) {
+	tmpDir := t.TempDir()
+
+	dns := DNS{
+		ConfigFile: tmpDir,
+		Hosts: HostsConfig{
+			Status: HostsStatusDisabled,
+		},
+	}
+	err := dns.validate()
+	assert.ErrorContains(t, err, "must be a regular file")
+}
+
+func TestDNS_ValidateConfigFile_EmptyFile(t *testing.T) {
+	tmpFile := createTempCorefile(t, "")
+
+	dns := DNS{
+		ConfigFile: tmpFile,
+		Hosts: HostsConfig{
+			Status: HostsStatusDisabled,
+		},
+	}
+	err := dns.validate()
+	assert.ErrorContains(t, err, "is empty")
+}
+
+func TestDNS_ValidateConfigFile_ExceedsSizeLimit(t *testing.T) {
+	tmpDir := t.TempDir()
+	tmpFile := filepath.Join(tmpDir, "Corefile")
+	// 1 MiB + 1 byte
+	data := make([]byte, 1048576+1)
+	require.NoError(t, os.WriteFile(tmpFile, data, 0644))
+
+	dns := DNS{
+		ConfigFile: tmpFile,
+		Hosts: HostsConfig{
+			Status: HostsStatusDisabled,
+		},
+	}
+	err := dns.validate()
+	assert.ErrorContains(t, err, "exceeds 1MiB size limit")
+}
+
+func TestDNS_ValidateConfigFile_ValidFile(t *testing.T) {
+	tmpFile := createTempCorefile(t, ".:5353 {\n    whoami\n    reload\n}\n")
+
+	dns := DNS{
+		ConfigFile: tmpFile,
+		Hosts: HostsConfig{
+			Status: HostsStatusDisabled,
+		},
+	}
+	assert.NoError(t, dns.validate())
+}
+
+func TestDNS_ConfigFile_IncorporatedFromDropIn(t *testing.T) {
+	tmpFile := createTempCorefile(t, ".:5353 {\n    whoami\n    reload\n}\n")
+
+	yamlConfig := fmt.Sprintf("dns:\n  configFile: %s\n", tmpFile)
+	config, err := getActiveConfigFromYAMLDropins([][]byte{[]byte(yamlConfig)})
+	require.NoError(t, err)
+	assert.Equal(t, tmpFile, config.DNS.ConfigFile)
+}
+
+func createTempCorefile(t *testing.T, content string) string {
+	t.Helper()
+	tmpDir := t.TempDir()
+	tmpFile := filepath.Join(tmpDir, "Corefile")
+	require.NoError(t, os.WriteFile(tmpFile, []byte(content), 0644))
+	return tmpFile
+}
diff --git a/pkg/controllers/dnsconfigurationwatcher.go b/pkg/controllers/dnsconfigurationwatcher.go
new file mode 100644
index 0000000000..66908fd588
--- /dev/null
+++ b/pkg/controllers/dnsconfigurationwatcher.go
@@ -0,0 +1,33 @@
+package controllers
+
+import (
+	"github.com/fsnotify/fsnotify"
+	"github.com/openshift/microshift/pkg/config"
+)
+
+type DNSConfigurationWatcherManager struct {
+	fileWatcher
+}
+
+func NewDNSConfigurationWatcherManager(cfg *config.Config) *DNSConfigurationWatcherManager {
+	return &DNSConfigurationWatcherManager{fileWatcher{cfg: fileWatcherConfig{
+		serviceName:        "dns-configuration-watcher-manager",
+		dependencies:       []string{"infrastructure-services-manager"},
+		file:               cfg.DNS.ConfigFile,
+		kubeconfig:         cfg.KubeConfigPath(config.KubeAdmin),
+		enabled:            cfg.DNS.ConfigFile != "",
+		configMapNamespace: "openshift-dns",
+		configMapName:      "dns-default",
+		configMapDataKey:   "Corefile",
+		labels: map[string]string{
+			"dns.operator.openshift.io/owning-dns": "default",
+		},
+		annotations: map[string]string{
+			"microshift.io/dns-config-file": cfg.DNS.ConfigFile,
+		},
+		eventMask:        fsnotify.Write | fsnotify.Create | fsnotify.Rename | fsnotify.Remove,
+		reAddOnCreate:    true,
+		mergeAnnotations: true,
+		deleteOnDisable:  false,
+	}}}
+}
diff --git a/pkg/controllers/filewatcher.go b/pkg/controllers/filewatcher.go
new file mode 100644
index 0000000000..fe132eed94
--- /dev/null
+++ b/pkg/controllers/filewatcher.go
@@ -0,0 +1,284 @@
+package controllers
+
+import (
+	"context"
+	"crypto/sha256"
+	"fmt"
+	"os"
+	"path/filepath"
+	"time"
+
+	"github.com/fsnotify/fsnotify"
+	corev1 "k8s.io/api/core/v1"
+	apierrors "k8s.io/apimachinery/pkg/api/errors"
+	metav1 "k8s.io/apimachinery/pkg/apis/meta/v1"
+	"k8s.io/client-go/kubernetes"
+	"k8s.io/client-go/tools/clientcmd"
+	"k8s.io/klog/v2"
+)
+
+type fileWatcherConfig struct {
+	serviceName        string
+	dependencies       []string
+	file               string
+	kubeconfig         string
+	enabled            bool
+	configMapNamespace string
+	configMapName      string
+	configMapDataKey   string
+	labels             map[string]string
+	annotations        map[string]string
+	eventMask          fsnotify.Op
+	reAddOnCreate      bool
+	mergeAnnotations   bool
+	deleteOnDisable    bool
+}
+
+type fileWatcher struct {
+	cfg fileWatcherConfig
+}
+
+func (fw *fileWatcher) Name() string           { return fw.cfg.serviceName }
+func (fw *fileWatcher) Dependencies() []string { return fw.cfg.dependencies }
+
+func (fw *fileWatcher) Run(ctx context.Context, ready chan<- struct{}, stopped chan<- struct{}) error {
+	defer close(stopped)
+
+	if !fw.cfg.enabled {
+		klog.Infof("%s is disabled (not configured)", fw.Name())
+		fw.cleanupOnDisable(ctx)
+		close(ready)
+		return ctx.Err()
+	}
+
+	kubeClient, err := fw.createKubeClient()
+	if err != nil {
+		klog.Errorf("%s failed to create Kubernetes client: %v", fw.Name(), err)
+		return err
+	}
+
+	if err := fw.updateConfigMap(ctx, kubeClient); err != nil {
+		klog.Errorf("%s failed to create initial ConfigMap: %v", fw.Name(), err)
+		return err
+	}
+
+	watcher, err := fsnotify.NewWatcher()
+	if err != nil {
+		klog.Errorf("%s failed to create file watcher: %v", fw.Name(), err)
+		return err
+	}
+	defer func() {
+		if cerr := watcher.Close(); cerr != nil {
+			klog.Errorf("%s failed to close file watcher: %v", fw.Name(), cerr)
+		}
+	}()
+
+	if err := fw.setupWatches(watcher); err != nil {
+		return err
+	}
+	close(ready)
+
+	lastHash, err := fw.getFileHash()
+	if err != nil {
+		klog.Warningf("%s failed to get initial file hash: %v", fw.Name(), err)
+	}
+
+	klog.Infof("%s is ready and watching %s", fw.Name(), fw.cfg.file)
+
+	return fw.eventLoop(ctx, watcher, kubeClient, lastHash)
+}
+
+func (fw *fileWatcher) setupWatches(watcher *fsnotify.Watcher) error {
+	filesToWatch := []string{
+		fw.cfg.file,
+		filepath.Dir(fw.cfg.file),
+	}
+	for i, file := range filesToWatch {
+		if err := watcher.Add(file); err != nil {
+			if i == 0 {
+				klog.Errorf("%s failed to watch file %s: %v", fw.Name(), fw.cfg.file, err)
+				return err
+			}
+			klog.Warningf("%s failed to watch directory %s: %v", fw.Name(), file, err)
+		}
+	}
+	return nil
+}
+
+func (fw *fileWatcher) eventLoop(ctx context.Context, watcher *fsnotify.Watcher, kubeClient kubernetes.Interface, initHash string) error {
+	lastHash := initHash
+
+	for {
+		select {
+		case <-ctx.Done():
+			klog.Infof("%s stopping", fw.Name())
+			return ctx.Err()
+
+		case event, ok := <-watcher.Events:
+			if !ok {
+				return fmt.Errorf("%s watcher channel closed", fw.Name())
+			}
+			if fw.isRelevantEvent(event) {
+				if fw.cfg.reAddOnCreate && event.Op&fsnotify.Create == fsnotify.Create {
+					_ = watcher.Add(fw.cfg.file)
+				}
+				updated, newHash, updateErr := fw.handleChange(ctx, kubeClient, lastHash)
+				if updateErr != nil {
+					klog.Errorf("%s failed to process file change: %v", fw.Name(), updateErr)
+					continue
+				}
+				if updated {
+					lastHash = newHash
+				}
+			}
+
+		case err, ok := <-watcher.Errors:
+			if !ok {
+				return fmt.Errorf("%s watcher error channel closed", fw.Name())
+			}
+			klog.Errorf("%s watcher error: %v", fw.Name(), err)
+		}
+	}
+}
+
+func (fw *fileWatcher) isRelevantEvent(event fsnotify.Event) bool {
+	if event.Name != fw.cfg.file {
+		return false
+	}
+	return event.Op&fw.cfg.eventMask != 0
+}
+
+func (fw *fileWatcher) handleChange(ctx context.Context, kubeClient kubernetes.Interface, lastHash string) (bool, string, error) {
+	klog.Infof("%s detected change in %s", fw.Name(), fw.cfg.file)
+	if _, err := os.Stat(fw.cfg.file); os.IsNotExist(err) {
+		klog.Warningf("%s watched file %s was removed, keeping last known ConfigMap content", fw.Name(), fw.cfg.file)
+		return false, lastHash, err
+	}
+	currentHash, err := fw.getFileHash()
+	if err != nil {
+		klog.Warningf("%s failed to get file hash after change: %v", fw.Name(), err)
+		return false, lastHash, err
+	}
+	if currentHash == lastHash {
+		klog.V(2).Infof("%s file hash unchanged, skipping update", fw.Name())
+		return false, lastHash, nil
+	}
+	if err := fw.updateConfigMap(ctx, kubeClient); err != nil {
+		klog.Errorf("%s failed to update ConfigMap: %v", fw.Name(), err)
+		return false, lastHash, err
+	}
+	klog.Infof("%s successfully updated ConfigMap %s/%s", fw.Name(), fw.cfg.configMapNamespace, fw.cfg.configMapName)
+	return true, currentHash, nil
+}
+
+func (fw *fileWatcher) createKubeClient() (*kubernetes.Clientset, error) {
+	cfg, err := clientcmd.BuildConfigFromFlags("", fw.cfg.kubeconfig)
+	if err != nil {
+		return nil, fmt.Errorf("failed to build kubeconfig: %w", err)
+	}
+	client, err := kubernetes.NewForConfig(cfg)
+	if err != nil {
+		return nil, fmt.Errorf("failed to create Kubernetes client: %w", err)
+	}
+	return client, nil
+}
+
+func (fw *fileWatcher) updateConfigMap(ctx context.Context, client kubernetes.Interface) error {
+	content, err := os.ReadFile(fw.cfg.file)
+	if err != nil {
+		return fmt.Errorf("failed to read file %s: %w", fw.cfg.file, err)
+	}
+	return fw.createOrUpdateConfigMap(ctx, client, string(content))
+}
+
+func (fw *fileWatcher) createOrUpdateConfigMap(ctx context.Context, client kubernetes.Interface, content string) error {
+	annotations := fw.buildAnnotations()
+	configMap := &corev1.ConfigMap{
+		ObjectMeta: metav1.ObjectMeta{
+			Name:        fw.cfg.configMapName,
+			Namespace:   fw.cfg.configMapNamespace,
+			Labels:      fw.cfg.labels,
+			Annotations: annotations,
+		},
+		Data: map[string]string{
+			fw.cfg.configMapDataKey: content,
+		},
+	}
+
+	configMapsClient := client.CoreV1().ConfigMaps(fw.cfg.configMapNamespace)
+
+	existing, err := configMapsClient.Get(ctx, fw.cfg.configMapName, metav1.GetOptions{})
+	switch {
+	case apierrors.IsNotFound(err):
+		if _, err = configMapsClient.Create(ctx, configMap, metav1.CreateOptions{}); err != nil {
+			return fmt.Errorf("failed to create ConfigMap: %w", err)
+		}
+		klog.Infof("%s created ConfigMap %s/%s", fw.Name(), fw.cfg.configMapNamespace, fw.cfg.configMapName)
+	case err != nil:
+		return fmt.Errorf("failed to get ConfigMap: %w", err)
+	default:
+		existing.Data = configMap.Data
+		if fw.cfg.mergeAnnotations {
+			if existing.Annotations == nil {
+				existing.Annotations = map[string]string{}
+			}
+			for k, v := range annotations {
+				existing.Annotations[k] = v
+			}
+		} else {
+			existing.Annotations = annotations
+		}
+		if _, err = configMapsClient.Update(ctx, existing, metav1.UpdateOptions{}); err != nil {
+			return fmt.Errorf("failed to update ConfigMap: %w", err)
+		}
+		klog.V(2).Infof("%s updated ConfigMap %s/%s", fw.Name(), fw.cfg.configMapNamespace, fw.cfg.configMapName)
+	}
+
+	return nil
+}
+
+func (fw *fileWatcher) buildAnnotations() map[string]string {
+	annotations := make(map[string]string, len(fw.cfg.annotations)+1)
+	for k, v := range fw.cfg.annotations {
+		annotations[k] = v
+	}
+	annotations["microshift.io/last-updated"] = time.Now().Format(time.RFC3339)
+	return annotations
+}
+
+func (fw *fileWatcher) cleanupOnDisable(ctx context.Context) {
+	if !fw.cfg.deleteOnDisable {
+		return
+	}
+	kubeClient, err := fw.createKubeClient()
+	if err != nil {
+		klog.Warningf("%s could not create Kubernetes client to delete ConfigMap: %v", fw.Name(), err)
+		return
+	}
+	if err := fw.deleteConfigMap(ctx, kubeClient); err != nil {
+		klog.Warningf("%s failed to delete ConfigMap when disabled: %v", fw.Name(), err)
+	}
+}
+
+func (fw *fileWatcher) deleteConfigMap(ctx context.Context, client kubernetes.Interface) error {
+	configMapsClient := client.CoreV1().ConfigMaps(fw.cfg.configMapNamespace)
+	err := configMapsClient.Delete(ctx, fw.cfg.configMapName, metav1.DeleteOptions{})
+	if err != nil {
+		if apierrors.IsNotFound(err) {
+			klog.V(2).Infof("%s ConfigMap %s/%s does not exist, nothing to delete", fw.Name(), fw.cfg.configMapNamespace, fw.cfg.configMapName)
+			return nil
+		}
+		return fmt.Errorf("failed to delete ConfigMap: %w", err)
+	}
+	klog.Infof("%s deleted ConfigMap %s/%s", fw.Name(), fw.cfg.configMapNamespace, fw.cfg.configMapName)
+	return nil
+}
+
+func (fw *fileWatcher) getFileHash() (string, error) {
+	content, err := os.ReadFile(fw.cfg.file)
+	if err != nil {
+		return "", err
+	}
+	hash := sha256.Sum256(content)
+	return fmt.Sprintf("%x", hash), nil
+}
diff --git a/pkg/controllers/hostswatcher.go b/pkg/controllers/hostswatcher.go
index f666cd3e90..9ff4f36996 100644
--- a/pkg/controllers/hostswatcher.go
+++ b/pkg/controllers/hostswatcher.go
@@ -1,280 +1,36 @@
 package controllers
 
 import (
-	"context"
-	"crypto/sha256"
-	"fmt"
-	"os"
-	"path/filepath"
-	"time"
-
 	"github.com/fsnotify/fsnotify"
 	"github.com/openshift/microshift/pkg/config"
-	corev1 "k8s.io/api/core/v1"
-	apierrors "k8s.io/apimachinery/pkg/api/errors"
-	metav1 "k8s.io/apimachinery/pkg/apis/meta/v1"
-	"k8s.io/client-go/kubernetes"
-	"k8s.io/client-go/tools/clientcmd"
-	"k8s.io/klog/v2"
-)
-
-const (
-	targetNameSpace = "openshift-dns"
-	configMapName   = "hosts-file"
 )
 
 type HostsWatcherManager struct {
-	file       string
-	status     config.HostsStatusEnum
-	kubeconfig string
+	fileWatcher
 }
 
 func NewHostsWatcherManager(cfg *config.Config) *HostsWatcherManager {
-	return &HostsWatcherManager{
-		file:       cfg.DNS.Hosts.File,
-		status:     cfg.DNS.Hosts.Status,
-		kubeconfig: cfg.KubeConfigPath(config.KubeAdmin),
-	}
-}
-
-func (s *HostsWatcherManager) Name() string           { return "hosts-watcher-manager" }
-func (s *HostsWatcherManager) Dependencies() []string { return []string{"kube-apiserver"} }
-
-func (s *HostsWatcherManager) Run(ctx context.Context, ready chan<- struct{}, stopped chan<- struct{}) error {
-	defer close(stopped)
-
-	if s.status != config.HostsStatusEnabled {
-		klog.Infof("%s is disabled (not configured)", s.Name())
-		// Delete ConfigMap if it exists when service is disabled
-		if kubeClient, err := s.createKubeClient(); err == nil {
-			if err := s.deleteConfigMap(ctx, kubeClient); err != nil {
-				klog.Warningf("%s failed to delete ConfigMap when disabled: %v", s.Name(), err)
-			}
-		} else {
-			klog.Warningf("%s could not create Kubernetes client to delete ConfigMap: %v", s.Name(), err)
-		}
-		defer close(ready)
-		return ctx.Err()
-	}
-
-	kubeClient, err := s.createKubeClient()
-	if err != nil {
-		klog.Errorf("%s failed to create Kubernetes client: %v", s.Name(), err)
-		return err
-	}
-
-	if err := s.updateConfigMaps(ctx, kubeClient); err != nil {
-		klog.Errorf("%s failed to create initial ConfigMaps: %v", s.Name(), err)
-		return err
-	}
-
-	watcher, err := fsnotify.NewWatcher()
-	if err != nil {
-		klog.Errorf("%s failed to create file watcher: %v", s.Name(), err)
-		return err
-	}
-	defer func() {
-		if cerr := watcher.Close(); cerr != nil {
-			klog.Errorf("%s failed to close file watcher: %v", s.Name(), cerr)
-		}
-	}()
-
-	if err := s.setupWatches(watcher); err != nil {
-		return err
-	}
-	close(ready)
-	klog.Infof("%s ready and watching for changes", s.Name())
-
-	lastHash, err := s.getFileHash(s.file)
-	if err != nil {
-		klog.Warningf("%s failed to get initial file hash: %v", s.Name(), err)
-	}
-
-	klog.Infof("%s is ready", s.Name())
-
-	return s.eventLoop(ctx, watcher, kubeClient, lastHash)
-}
-
-func (s *HostsWatcherManager) setupWatches(watcher *fsnotify.Watcher) error {
-	filesToWatch := []string{
-		s.file,
-		filepath.Dir(s.file),
-	}
-	for i, file := range filesToWatch {
-		if err := watcher.Add(file); err != nil {
-			// Warn if directory, error out if file
-			if i == 0 {
-				klog.Errorf("%s failed to watch hosts file %s: %v", s.Name(), s.file, err)
-				return err
-			}
-			klog.Warningf("%s failed to watch hosts directory %s: %v", s.Name(), file, err)
-		}
-	}
-	return nil
-}
-
-func (s *HostsWatcherManager) eventLoop(ctx context.Context, watcher *fsnotify.Watcher, kubeClient kubernetes.Interface, initHash string) error {
-	lastHash := initHash
-
-	for {
-		select {
-		case <-ctx.Done():
-			klog.Infof("%s stopping", s.Name())
-			return watcher.Close()
-
-		case event, ok := <-watcher.Events:
-			if !ok {
-				return fmt.Errorf("%s watcher channel closed", s.Name())
-			}
-			if s.isRelevantHostsEvent(event) {
-				updated, newHash, updateErr := s.handleHostsChange(ctx, kubeClient, lastHash)
-				if updateErr != nil {
-					klog.Errorf("%s failed to process hosts file change: %v", s.Name(), updateErr)
-					continue
-				}
-				if updated {
-					lastHash = newHash
-				}
-			}
-
-		case err, ok := <-watcher.Errors:
-			if !ok {
-				return fmt.Errorf("%s watcher error channel closed", s.Name())
-			}
-			klog.Errorf("%s watcher error: %v", s.Name(), err)
-		}
-	}
-}
-
-func (s *HostsWatcherManager) isRelevantHostsEvent(event fsnotify.Event) bool {
-	if event.Name != s.file {
-		return false
-	}
-	return event.Op&fsnotify.Write == fsnotify.Write || event.Op&fsnotify.Create == fsnotify.Create
-}
-
-func (s *HostsWatcherManager) handleHostsChange(ctx context.Context, kubeClient kubernetes.Interface, lastHash string) (bool, string, error) {
-	klog.Infof("%s detected change in hosts file: %s", s.Name(), s.file)
-	currentHash, err := s.getFileHash(s.file)
-	if err != nil {
-		klog.Warningf("%s failed to get file hash after change: %v", s.Name(), err)
-		return false, lastHash, err
-	}
-	if currentHash == lastHash {
-		klog.V(2).Infof("%s file hash unchanged, skipping update", s.Name())
-		return false, lastHash, nil
-	}
-	if err := s.updateConfigMaps(ctx, kubeClient); err != nil {
-		klog.Errorf("%s failed to update ConfigMaps: %v", s.Name(), err)
-		return false, currentHash, err
-	} else {
-		klog.Infof("%s successfully updated ConfigMaps in namespaces: %v", s.Name(), targetNameSpace)
-	}
-	return true, currentHash, nil
-}
-
-func (s *HostsWatcherManager) createKubeClient() (*kubernetes.Clientset, error) {
-	config, err := clientcmd.BuildConfigFromFlags("", s.kubeconfig)
-	if err != nil {
-		return nil, fmt.Errorf("failed to build kubeconfig: %w", err)
-	}
-
-	client, err := kubernetes.NewForConfig(config)
-	if err != nil {
-		return nil, fmt.Errorf("failed to create Kubernetes client: %w", err)
-	}
-
-	return client, nil
-}
-
-func (s *HostsWatcherManager) updateConfigMaps(ctx context.Context, client kubernetes.Interface) error {
-	hostsContent, err := s.readHostsFile()
-	if err != nil {
-		return fmt.Errorf("failed to read hosts file: %w", err)
-	}
-
-	if err := s.createOrUpdateConfigMap(ctx, client, targetNameSpace, hostsContent); err != nil {
-		klog.Errorf("%s failed to update ConfigMap in namespace %s: %v", s.Name(), targetNameSpace, err)
-	}
-
-	return nil
-}
-
-func (s *HostsWatcherManager) createOrUpdateConfigMap(ctx context.Context, client kubernetes.Interface, namespace string, hostsContent string) error {
-	configMap := &corev1.ConfigMap{
-		ObjectMeta: metav1.ObjectMeta{
-			Name:      configMapName,
-			Namespace: namespace,
-			Labels: map[string]string{
-				"app.kubernetes.io/name":       "microshift-hosts-watcher",
-				"app.kubernetes.io/component":  "hosts-file-sync",
-				"app.kubernetes.io/managed-by": "microshift",
-				// Restrict access to only CoreDNS pods
-				"microshift.io/access-restricted": "coredns-only",
-			},
-			Annotations: map[string]string{
-				"microshift.io/hosts-file-path": s.file,
-				"microshift.io/last-updated":    time.Now().Format(time.RFC3339),
-			},
+	return &HostsWatcherManager{fileWatcher{cfg: fileWatcherConfig{
+		serviceName:        "hosts-watcher-manager",
+		dependencies:       []string{"infrastructure-services-manager"},
+		file:               cfg.DNS.Hosts.File,
+		kubeconfig:         cfg.KubeConfigPath(config.KubeAdmin),
+		enabled:            cfg.DNS.Hosts.Status == config.HostsStatusEnabled,
+		configMapNamespace: "openshift-dns",
+		configMapName:      "hosts-file",
+		configMapDataKey:   "hosts",
+		labels: map[string]string{
+			"app.kubernetes.io/name":          "microshift-hosts-watcher",
+			"app.kubernetes.io/component":     "hosts-file-sync",
+			"app.kubernetes.io/managed-by":    "microshift",
+			"microshift.io/access-restricted": "coredns-only",
 		},
-		Data: map[string]string{
-			"hosts": hostsContent,
+		annotations: map[string]string{
+			"microshift.io/hosts-file-path": cfg.DNS.Hosts.File,
 		},
-	}
-
-	configMapsClient := client.CoreV1().ConfigMaps(namespace)
-
-	// Try to get existing ConfigMap
-	existing, err := configMapsClient.Get(ctx, configMapName, metav1.GetOptions{})
-	if err != nil {
-		// ConfigMap doesn't exist, create it
-		_, err = configMapsClient.Create(ctx, configMap, metav1.CreateOptions{})
-		if err != nil {
-			return fmt.Errorf("failed to create ConfigMap: %w", err)
-		}
-		klog.Infof("%s created ConfigMap %s in namespace %s", s.Name(), configMapName, namespace)
-	} else {
-		// ConfigMap exists, update it
-		existing.Data = configMap.Data
-		existing.Annotations = configMap.Annotations
-		_, err = configMapsClient.Update(ctx, existing, metav1.UpdateOptions{})
-		if err != nil {
-			return fmt.Errorf("failed to update ConfigMap: %w", err)
-		}
-		klog.V(2).Infof("%s updated ConfigMap %s in namespace %s", s.Name(), configMapName, namespace)
-	}
-
-	return nil
-}
-
-func (s *HostsWatcherManager) readHostsFile() (string, error) {
-	content, err := os.ReadFile(s.file)
-	if err != nil {
-		return "", fmt.Errorf("failed to read hosts file %s: %w", s.file, err)
-	}
-	return string(content), nil
-}
-
-func (s *HostsWatcherManager) getFileHash(filePath string) (string, error) {
-	content, err := os.ReadFile(filePath)
-	if err != nil {
-		return "", err
-	}
-	hash := sha256.Sum256(content)
-	return fmt.Sprintf("%x", hash), nil
-}
-
-func (s *HostsWatcherManager) deleteConfigMap(ctx context.Context, client kubernetes.Interface) error {
-	configMapsClient := client.CoreV1().ConfigMaps(targetNameSpace)
-	err := configMapsClient.Delete(ctx, configMapName, metav1.DeleteOptions{})
-	if err != nil {
-		// If ConfigMap doesn't exist, that's fine - it's already deleted
-		if apierrors.IsNotFound(err) {
-			klog.V(2).Infof("%s ConfigMap %s in namespace %s does not exist, nothing to delete", s.Name(), configMapName, targetNameSpace)
-			return nil
-		}
-		return fmt.Errorf("failed to delete ConfigMap: %w", err)
-	}
-	klog.Infof("%s deleted ConfigMap %s in namespace %s", s.Name(), configMapName, targetNameSpace)
-	return nil
+		eventMask:        fsnotify.Write | fsnotify.Create,
+		reAddOnCreate:    false,
+		mergeAnnotations: false,
+		deleteOnDisable:  true,
+	}}}
 }
diff --git a/test/assets/dns/Corefile.template b/test/assets/dns/Corefile.template
new file mode 100644
index 0000000000..4039e7cc8b
--- /dev/null
+++ b/test/assets/dns/Corefile.template
@@ -0,0 +1,24 @@
+.:5353 {
+    bufsize 1232
+    errors
+    health {
+        lameduck 20s
+    }
+    ready
+    kubernetes cluster.local in-addr.arpa ip6.arpa {
+        pods insecure
+        fallthrough in-addr.arpa ip6.arpa
+    }
+    prometheus 127.0.0.1:9153
+    forward . /etc/resolv.conf {
+        policy sequential
+    }
+    cache 900 {
+        denial 9984 30
+    }
+    hosts {
+        ${COREFILE_HOST_IP} ${COREFILE_HOSTNAME}
+        fallthrough
+    }
+    reload
+}
diff --git a/test/resources/dns.resource b/test/resources/dns.resource
new file mode 100644
index 0000000000..46a494408b
--- /dev/null
+++ b/test/resources/dns.resource
@@ -0,0 +1,38 @@
+*** Settings ***
+Documentation       Shared keywords for DNS test suites
+
+Library             SSHLibrary
+Resource            oc.resource
+
+
+*** Keywords ***
+Resolve Host From Pod
+    [Documentation]    Verify DNS resolution from a pod using nslookup
+    [Arguments]    ${hostname}
+    Wait Until Keyword Succeeds    40x    5s
+    ...    Router Should Resolve Hostname    ${hostname}
+
+Router Should Resolve Hostname
+    [Documentation]    Check if the router pod resolves the given hostname
+    [Arguments]    ${hostname}
+    ${output}=    Oc Exec    router-default    nslookup ${hostname}    openshift-ingress    deployment
+    Should Contain    ${output}    Name:
+    Should Contain    ${output}    ${hostname}
+
+Add Fake IP To NIC
+    [Documentation]    Add the given IP to br-ex temporarily.
+    [Arguments]    ${ip_address}    ${nic_name}=br-ex
+    ${stdout}    ${stderr}    ${rc}=    SSHLibrary.Execute Command
+    ...    ip address add ${ip_address}/32 dev ${nic_name}
+    ...    sudo=True    return_rc=True    return_stderr=True    return_stdout=True
+    Log Many    ${stdout}    ${stderr}
+    Should Be Equal As Integers    0    ${rc}
+
+Remove Fake IP From NIC
+    [Documentation]    Remove the given IP from br-ex.
+    [Arguments]    ${ip_address}    ${nic_name}=br-ex
+    ${stdout}    ${stderr}    ${rc}=    SSHLibrary.Execute Command
+    ...    ip address delete ${ip_address}/32 dev ${nic_name}
+    ...    sudo=True    return_rc=True    return_stderr=True    return_stdout=True
+    Log Many    ${stdout}    ${stderr}
+    Should Be Equal As Integers    0    ${rc}
diff --git a/test/suites/standard1/dns-custom-config.robot b/test/suites/standard1/dns-custom-config.robot
new file mode 100644
index 0000000000..ab05732521
--- /dev/null
+++ b/test/suites/standard1/dns-custom-config.robot
@@ -0,0 +1,129 @@
+*** Settings ***
+Documentation       Tests for custom DNS configuration (dns.configFile)
+
+Resource            ../../resources/common.resource
+Resource            ../../resources/oc.resource
+Resource            ../../resources/microshift-config.resource
+Resource            ../../resources/microshift-process.resource
+Resource            ../../resources/microshift-network.resource
+Resource            ../../resources/dns.resource
+Resource            ../../resources/hosts.resource
+Library             ../../resources/journalctl.py
+
+Suite Setup         Setup Suite With Namespace
+Suite Teardown      Teardown Suite With Namespace
+
+Test Tags           slow
+
+
+*** Variables ***
+${FAKE_LISTEN_IP}           99.99.99.98
+${CUSTOM_COREFILE_PATH}     /etc/microshift/dns/Corefile
+${COREFILE_TEMPLATE}        ./assets/dns/Corefile.template
+${HOSTNAME}                 ${EMPTY}
+
+${CUSTOM_DNS_CONFIG}        SEPARATOR=\n
+...                         ---
+...                         dns:
+...                         \ \ configFile: /etc/microshift/dns/Corefile
+
+
+*** Test Cases ***
+Custom DNS Config File Is Used By CoreDNS
+    [Documentation]    Provide a valid custom Corefile and verify CoreDNS uses it
+    ...    instead of the default template-rendered configuration.
+    [Setup]    Setup Custom Corefile With Hosts Entry
+    Verify ConfigMap Uses Custom Corefile
+    Resolve Host From Pod    ${HOSTNAME}
+    [Teardown]    Teardown Custom Corefile
+
+Runtime Reload Without MicroShift Restart
+    [Documentation]    Modify the custom Corefile while MicroShift is running
+    ...    and verify CoreDNS picks up the change without restart.
+    [Setup]    Setup Custom Corefile With Hosts Entry
+    Resolve Host From Pod    ${HOSTNAME}
+    ${updated_hostname}=    Generate Random HostName
+    Update Corefile With New Host    ${updated_hostname}
+    Wait Until Keyword Succeeds    20x    5s
+    ...    ConfigMap Should Contain Hostname    ${updated_hostname}
+    Resolve Host From Pod    ${updated_hostname}
+    [Teardown]    Teardown Custom Corefile
+
+ConfigMap Unchanged After Corefile Removal
+    [Documentation]    Remove the custom Corefile while MicroShift is running
+    ...    and verify the ConfigMap retains the last known content.
+    [Setup]    Setup Custom Corefile With Hosts Entry
+    Verify ConfigMap Uses Custom Corefile
+    ${cursor}=    Get Journal Cursor
+    Remove Custom Corefile
+    Pattern Should Appear In Log Output
+    ...    ${cursor}    watched file.*was removed, keeping last known ConfigMap content
+    ConfigMap Should Contain Hostname    ${HOSTNAME}
+    [Teardown]    Teardown Custom Corefile
+
+Cluster Local Resolution With Custom Corefile
+    [Documentation]    Verify that a custom Corefile with the kubernetes plugin
+    ...    still resolves cluster-local services correctly.
+    [Setup]    Setup Custom Corefile With Hosts Entry
+    Resolve Host From Pod    kubernetes.default.svc.cluster.local
+    [Teardown]    Teardown Custom Corefile
+
+
+*** Keywords ***
+Build Custom Corefile
+    [Documentation]    Build a Corefile from the template file, substituting
+    ...    the hostname and IP placeholders.
+    [Arguments]    ${hostname}    ${ip}
+    ${template}=    OperatingSystem.Get File    ${COREFILE_TEMPLATE}
+    VAR    ${COREFILE_HOSTNAME}=    ${hostname}
+    VAR    ${COREFILE_HOST_IP}=    ${ip}
+    ${corefile}=    Replace Variables    ${template}
+    RETURN    ${corefile}
+
+Setup Custom Corefile With Hosts Entry
+    [Documentation]    Create a custom Corefile with a fake hostname entry,
+    ...    upload it, configure MicroShift to use it, and restart.
+    ${HOSTNAME}=    Generate Random HostName
+    VAR    ${HOSTNAME}=    ${HOSTNAME}    scope=SUITE
+    Add Fake IP To NIC    ${FAKE_LISTEN_IP}
+    ${corefile}=    Build Custom Corefile    ${HOSTNAME}    ${FAKE_LISTEN_IP}
+    Create Remote Dir For Path    ${CUSTOM_COREFILE_PATH}
+    Upload String To File    ${corefile}    ${CUSTOM_COREFILE_PATH}
+    Drop In MicroShift Config    ${CUSTOM_DNS_CONFIG}    20-dns-custom
+    Restart MicroShift
+
+Update Corefile With New Host
+    [Documentation]    Add a new hosts entry to the custom Corefile without
+    ...    restarting MicroShift. The file watcher and CoreDNS reload plugin
+    ...    should pick up the change.
+    [Arguments]    ${hostname}
+    ${corefile}=    Build Custom Corefile    ${hostname}    ${FAKE_LISTEN_IP}
+    Upload String To File    ${corefile}    ${CUSTOM_COREFILE_PATH}
+
+Verify ConfigMap Uses Custom Corefile
+    [Documentation]    Verify the dns-default ConfigMap contains custom content
+    ...    rather than the default template-rendered Corefile.
+    Wait Until Keyword Succeeds    20x    5s
+    ...    ConfigMap Should Contain Hostname    ${HOSTNAME}
+
+ConfigMap Should Contain Hostname
+    [Documentation]    Check the dns-default ConfigMap Corefile data for the hostname
+    [Arguments]    ${hostname}
+    ${corefile_data}=    Oc Get JsonPath
+    ...    configmap    openshift-dns    dns-default    .data.Corefile
+    Should Contain    ${corefile_data}    ${hostname}
+
+Teardown Custom Corefile
+    [Documentation]    Remove custom Corefile, drop-in config, fake IP, and restart
+    Run Keywords
+    ...    Remove Drop In MicroShift Config    20-dns-custom
+    ...    AND    Remove Custom Corefile
+    ...    AND    Remove Fake IP From NIC    ${FAKE_LISTEN_IP}
+    ...    AND    Restart MicroShift
+
+Remove Custom Corefile
+    [Documentation]    Remove the custom Corefile from the host
+    ${stdout}    ${stderr}    ${rc}=    Execute Command
+    ...    rm -f ${CUSTOM_COREFILE_PATH}
+    ...    sudo=True    return_rc=True    return_stdout=True    return_stderr=True
+    Should Be Equal As Integers    0    ${rc}
diff --git a/test/suites/standard1/dns.robot b/test/suites/standard1/dns.robot
index 84a690ccac..5d22c4d5cb 100644
--- a/test/suites/standard1/dns.robot
+++ b/test/suites/standard1/dns.robot
@@ -4,6 +4,7 @@ Documentation       Core DNS smoke tests
 Resource            ../../resources/common.resource
 Resource            ../../resources/oc.resource
 Resource            ../../resources/microshift-network.resource
+Resource            ../../resources/dns.resource
 Resource            ../../resources/microshift-config.resource
 Resource            ../../resources/microshift-process.resource
 Resource            ../../resources/hosts.resource
@@ -91,18 +92,6 @@ Get Hosts Config Custom
     END
     RETURN    ${config}
 
-Resolve Host From Pod
-    [Documentation]    Resolve host from pod
-    [Arguments]    ${hostname}
-    Wait Until Keyword Succeeds    40x    5s
-    ...    Router Should Resolve Hostname    ${hostname}
-
-Router Should Resolve Hostname
-    [Documentation]    Check if the router pod resolves the given hostname
-    [Arguments]    ${hostname}
-    ${fuse_device}=    Oc Exec    router-default    nslookup ${hostname}    openshift-ingress    deployment
-    Should Contain    ${fuse_device}    Name:    ${hostname}
-
 Setup With Custom Config
     [Documentation]    Install a custom config and restart MicroShift
     [Arguments]    ${config_content}    ${hostsFile}
@@ -128,24 +117,6 @@ Teardown Hosts File
     ...    AND
     ...    Remove Drop In MicroShift Config    20-dns
 
-Add Fake IP To NIC
-    [Documentation]    Add the given IP to the given NIC temporarily.
-    [Arguments]    ${ip_address}=${FAKE_LISTEN_IP}    ${nic_name}=br-ex
-    ${stdout}    ${stderr}    ${rc}=    SSHLibrary.Execute Command
-    ...    ip address add ${ip_address}/32 dev ${nic_name}
-    ...    sudo=True    return_rc=True    return_stderr=True    return_stdout=True
-    Log Many    ${stdout}    ${stderr}
-    Should Be Equal As Integers    0    ${rc}
-
-Remove Fake IP From NIC
-    [Documentation]    Remove the given IP from the given NIC.
-    [Arguments]    ${ip_address}=${FAKE_LISTEN_IP}    ${nic_name}=br-ex
-    ${stdout}    ${stderr}    ${rc}=    SSHLibrary.Execute Command
-    ...    ip address delete ${ip_address}/32 dev ${nic_name}
-    ...    sudo=True    return_rc=True    return_stderr=True    return_stdout=True
-    Log Many    ${stdout}    ${stderr}
-    Should Be Equal As Integers    0    ${rc}
-
 Check CoreDNS Hosts Feature
     [Documentation]    Skip suite if CoreDNS hosts feature is not available
     ${config}=    Show Config    default