diff --git a/libcontainer/cgroups/systemd/common.go b/libcontainer/cgroups/systemd/common.go
index 6d5def712..268b713c0 100644
--- a/libcontainer/cgroups/systemd/common.go
+++ b/libcontainer/cgroups/systemd/common.go
@@ -28,10 +28,6 @@ const (
 )
 
 var (
-	connOnce sync.Once
-	connDbus *systemdDbus.Conn
-	connErr  error
-
 	versionOnce sync.Once
 	version     int
 
@@ -291,19 +287,6 @@ func generateDeviceProperties(rules []*devices.Rule) ([]systemdDbus.Property, er
 	return properties, nil
 }
 
-// getDbusConnection lazy initializes systemd dbus connection
-// and returns it
-func getDbusConnection(rootless bool) (*systemdDbus.Conn, error) {
-	connOnce.Do(func() {
-		if rootless {
-			connDbus, connErr = NewUserSystemdDbus()
-		} else {
-			connDbus, connErr = systemdDbus.New()
-		}
-	})
-	return connDbus, connErr
-}
-
 func newProp(name string, units interface{}) systemdDbus.Property {
 	return systemdDbus.Property{
 		Name:  name,
@@ -319,19 +302,29 @@ func getUnitName(c *configs.Cgroup) string {
 	return c.Name
 }
 
-// isUnitExists returns true if the error is that a systemd unit already exists.
-func isUnitExists(err error) bool {
+// isDbusError returns true if the error is a specific dbus error.
+func isDbusError(err error, name string) bool {
 	if err != nil {
-		if dbusError, ok := err.(dbus.Error); ok {
-			return strings.Contains(dbusError.Name, "org.freedesktop.systemd1.UnitExists")
+		var derr *dbus.Error
+		if errors.As(err, &derr) {
+			return strings.Contains(derr.Name, name)
 		}
 	}
 	return false
 }
 
-func startUnit(dbusConnection *systemdDbus.Conn, unitName string, properties []systemdDbus.Property) error {
+// isUnitExists returns true if the error is that a systemd unit already exists.
+func isUnitExists(err error) bool {
+	return isDbusError(err, "org.freedesktop.systemd1.UnitExists")
+}
+
+func startUnit(cm *dbusConnManager, unitName string, properties []systemdDbus.Property) error {
 	statusChan := make(chan string, 1)
-	if _, err := dbusConnection.StartTransientUnit(unitName, "replace", properties, statusChan); err == nil {
+	err := cm.retryOnDisconnect(func(c *systemdDbus.Conn) error {
+		_, err := c.StartTransientUnit(unitName, "replace", properties, statusChan)
+		return err
+	})
+	if err == nil {
 		timeout := time.NewTimer(30 * time.Second)
 		defer timeout.Stop()
 
@@ -340,11 +333,11 @@ func startUnit(dbusConnection *systemdDbus.Conn, unitName string, properties []s
 			close(statusChan)
 			// Please refer to https://godoc.org/github.com/coreos/go-systemd/dbus#Conn.StartUnit
 			if s != "done" {
-				dbusConnection.ResetFailedUnit(unitName)
+				resetFailedUnit(cm, unitName)
 				return errors.Errorf("error creating systemd unit `%s`: got `%s`", unitName, s)
 			}
 		case <-timeout.C:
-			dbusConnection.ResetFailedUnit(unitName)
+			resetFailedUnit(cm, unitName)
 			return errors.New("Timeout waiting for systemd to create " + unitName)
 		}
 	} else if !isUnitExists(err) {
@@ -354,9 +347,13 @@ func startUnit(dbusConnection *systemdDbus.Conn, unitName string, properties []s
 	return nil
 }
 
-func stopUnit(dbusConnection *systemdDbus.Conn, unitName string) error {
+func stopUnit(cm *dbusConnManager, unitName string) error {
 	statusChan := make(chan string, 1)
-	if _, err := dbusConnection.StopUnit(unitName, "replace", statusChan); err == nil {
+	err := cm.retryOnDisconnect(func(c *systemdDbus.Conn) error {
+		_, err := c.StopUnit(unitName, "replace", statusChan)
+		return err
+	})
+	if err == nil {
 		select {
 		case s := <-statusChan:
 			close(statusChan)
@@ -371,10 +368,30 @@ func stopUnit(dbusConnection *systemdDbus.Conn, unitName string) error {
 	return nil
 }
 
-func systemdVersion(conn *systemdDbus.Conn) int {
+func resetFailedUnit(cm *dbusConnManager, name string) {
+	err := cm.retryOnDisconnect(func(c *systemdDbus.Conn) error {
+		return c.ResetFailedUnit(name)
+	})
+	if err != nil {
+		logrus.Warnf("unable to reset failed unit: %v", err)
+	}
+}
+
+func setUnitProperties(cm *dbusConnManager, name string, properties ...systemdDbus.Property) error {
+	return cm.retryOnDisconnect(func(c *systemdDbus.Conn) error {
+		return c.SetUnitProperties(name, true, properties...)
+	})
+}
+
+func systemdVersion(cm *dbusConnManager) int {
 	versionOnce.Do(func() {
 		version = -1
-		verStr, err := conn.GetManagerProperty("Version")
+		var verStr string
+		err := cm.retryOnDisconnect(func(c *systemdDbus.Conn) error {
+			var err error
+			verStr, err = c.GetManagerProperty("Version")
+			return err
+		})
 		if err == nil {
 			version, err = systemdVersionAtoi(verStr)
 		}
@@ -402,10 +419,10 @@ func systemdVersionAtoi(verStr string) (int, error) {
 	return ver, errors.Wrapf(err, "can't parse version %s", verStr)
 }
 
-func addCpuQuota(conn *systemdDbus.Conn, properties *[]systemdDbus.Property, quota int64, period uint64) {
+func addCpuQuota(cm *dbusConnManager, properties *[]systemdDbus.Property, quota int64, period uint64) {
 	if period != 0 {
 		// systemd only supports CPUQuotaPeriodUSec since v242
-		sdVer := systemdVersion(conn)
+		sdVer := systemdVersion(cm)
 		if sdVer >= 242 {
 			*properties = append(*properties,
 				newProp("CPUQuotaPeriodUSec", period))
@@ -436,13 +453,13 @@ func addCpuQuota(conn *systemdDbus.Conn, properties *[]systemdDbus.Property, quo
 	}
 }
 
-func addCpuset(conn *systemdDbus.Conn, props *[]systemdDbus.Property, cpus, mems string) error {
+func addCpuset(cm *dbusConnManager, props *[]systemdDbus.Property, cpus, mems string) error {
 	if cpus == "" && mems == "" {
 		return nil
 	}
 
 	// systemd only supports AllowedCPUs/AllowedMemoryNodes since v244
-	sdVer := systemdVersion(conn)
+	sdVer := systemdVersion(cm)
 	if sdVer < 244 {
 		logrus.Debugf("systemd v%d is too old to support AllowedCPUs/AllowedMemoryNodes"+
 			" (settings will still be applied to cgroupfs)", sdVer)
diff --git a/libcontainer/cgroups/systemd/dbus.go b/libcontainer/cgroups/systemd/dbus.go
new file mode 100644
index 000000000..0297a3fc2
--- /dev/null
+++ b/libcontainer/cgroups/systemd/dbus.go
@@ -0,0 +1,89 @@
+// +build linux
+
+package systemd
+
+import (
+	"sync"
+
+	systemdDbus "github.com/coreos/go-systemd/v22/dbus"
+	dbus "github.com/godbus/dbus/v5"
+)
+
+type dbusConnManager struct {
+	conn     *systemdDbus.Conn
+	rootless bool
+	sync.RWMutex
+}
+
+// newDbusConnManager initializes systemd dbus connection manager.
+func newDbusConnManager(rootless bool) *dbusConnManager {
+	return &dbusConnManager{
+		rootless: rootless,
+	}
+}
+
+// getConnection lazily initializes and returns systemd dbus connection.
+func (d *dbusConnManager) getConnection() (*systemdDbus.Conn, error) {
+	// In the case where d.conn != nil
+	// Use the read lock the first time to ensure
+	// that Conn can be acquired at the same time.
+	d.RLock()
+	if conn := d.conn; conn != nil {
+		d.RUnlock()
+		return conn, nil
+	}
+	d.RUnlock()
+
+	// In the case where d.conn == nil
+	// Use write lock to ensure that only one
+	// will be created
+	d.Lock()
+	defer d.Unlock()
+	if conn := d.conn; conn != nil {
+		return conn, nil
+	}
+
+	conn, err := d.newConnection()
+	if err != nil {
+		return nil, err
+	}
+	d.conn = conn
+	return conn, nil
+}
+
+func (d *dbusConnManager) newConnection() (*systemdDbus.Conn, error) {
+	if d.rootless {
+		return newUserSystemdDbus()
+	}
+	return systemdDbus.New()
+}
+
+// resetConnection resets the connection to its initial state
+// (so it can be reconnected if necessary).
+func (d *dbusConnManager) resetConnection(conn *systemdDbus.Conn) {
+	d.Lock()
+	defer d.Unlock()
+	if d.conn != nil && d.conn == conn {
+		d.conn.Close()
+		d.conn = nil
+	}
+}
+
+var errDbusConnClosed = dbus.ErrClosed.Error()
+
+// retryOnDisconnect calls op, and if the error it returns is about closed dbus
+// connection, the connection is re-established and the op is retried. This helps
+// with the situation when dbus is restarted and we have a stale connection.
+func (d *dbusConnManager) retryOnDisconnect(op func(*systemdDbus.Conn) error) error {
+	for {
+		conn, err := d.getConnection()
+		if err != nil {
+			return err
+		}
+		err = op(conn)
+		if !isDbusError(err, errDbusConnClosed) {
+			return err
+		}
+		d.resetConnection(conn)
+	}
+}
diff --git a/libcontainer/cgroups/systemd/user.go b/libcontainer/cgroups/systemd/user.go
index 8fe916884..234df8e6b 100644
--- a/libcontainer/cgroups/systemd/user.go
+++ b/libcontainer/cgroups/systemd/user.go
@@ -17,8 +17,8 @@ import (
 	"github.com/pkg/errors"
 )
 
-// NewUserSystemdDbus creates a connection for systemd user-instance.
-func NewUserSystemdDbus() (*systemdDbus.Conn, error) {
+// newUserSystemdDbus creates a connection for systemd user-instance.
+func newUserSystemdDbus() (*systemdDbus.Conn, error) {
 	addr, err := DetectUserDbusSessionBusAddress()
 	if err != nil {
 		return nil, err
diff --git a/libcontainer/cgroups/systemd/v1.go b/libcontainer/cgroups/systemd/v1.go
index 64af1d94b..33ef97ee8 100644
--- a/libcontainer/cgroups/systemd/v1.go
+++ b/libcontainer/cgroups/systemd/v1.go
@@ -21,12 +21,14 @@ type legacyManager struct {
 	mu      sync.Mutex
 	cgroups *configs.Cgroup
 	paths   map[string]string
+	dbus    *dbusConnManager
 }
 
 func NewLegacyManager(cg *configs.Cgroup, paths map[string]string) cgroups.Manager {
 	return &legacyManager{
 		cgroups: cg,
 		paths:   paths,
+		dbus:    newDbusConnManager(false),
 	}
 }
 
@@ -57,7 +59,7 @@ var legacySubsystems = []subsystem{
 	&fs.NameGroup{GroupName: "name=systemd"},
 }
 
-func genV1ResourcesProperties(c *configs.Cgroup, conn *systemdDbus.Conn) ([]systemdDbus.Property, error) {
+func genV1ResourcesProperties(c *configs.Cgroup, cm *dbusConnManager) ([]systemdDbus.Property, error) {
 	var properties []systemdDbus.Property
 	r := c.Resources
 
@@ -77,7 +79,7 @@ func genV1ResourcesProperties(c *configs.Cgroup, conn *systemdDbus.Conn) ([]syst
 			newProp("CPUShares", r.CpuShares))
 	}
 
-	addCpuQuota(conn, &properties, r.CpuQuota, r.CpuPeriod)
+	addCpuQuota(cm, &properties, r.CpuQuota, r.CpuPeriod)
 
 	if r.BlkioWeight != 0 {
 		properties = append(properties,
@@ -90,7 +92,7 @@ func genV1ResourcesProperties(c *configs.Cgroup, conn *systemdDbus.Conn) ([]syst
 			newProp("TasksMax", uint64(r.PidsLimit)))
 	}
 
-	err = addCpuset(conn, &properties, r.CpusetCpus, r.CpusetMems)
+	err = addCpuset(cm, &properties, r.CpusetCpus, r.CpusetMems)
 	if err != nil {
 		return nil, err
 	}
@@ -164,11 +166,7 @@ func (m *legacyManager) Apply(pid int) error {
 	properties = append(properties,
 		newProp("DefaultDependencies", false))
 
-	dbusConnection, err := getDbusConnection(false)
-	if err != nil {
-		return err
-	}
-	resourcesProperties, err := genV1ResourcesProperties(c, dbusConnection)
+	resourcesProperties, err := genV1ResourcesProperties(c, m.dbus)
 	if err != nil {
 		return err
 	}
@@ -183,7 +181,7 @@ func (m *legacyManager) Apply(pid int) error {
 		}
 	}
 
-	if err := startUnit(dbusConnection, unitName, properties); err != nil {
+	if err := startUnit(m.dbus, unitName, properties); err != nil {
 		return err
 	}
 
@@ -221,13 +219,8 @@ func (m *legacyManager) Destroy() error {
 	m.mu.Lock()
 	defer m.mu.Unlock()
 
-	dbusConnection, err := getDbusConnection(false)
-	if err != nil {
-		return err
-	}
-	unitName := getUnitName(m.cgroups)
+	stopErr := stopUnit(m.dbus, getUnitName(m.cgroups))
 
-	stopErr := stopUnit(dbusConnection, unitName)
 	// Both on success and on error, cleanup all the cgroups we are aware of.
 	// Some of them were created directly by Apply() and are not managed by systemd.
 	if err := cgroups.RemovePaths(m.paths); err != nil {
@@ -354,11 +347,7 @@ func (m *legacyManager) Set(container *configs.Config) error {
 	if container.Cgroups.Resources.Unified != nil {
 		return cgroups.ErrV1NoUnified
 	}
-	dbusConnection, err := getDbusConnection(false)
-	if err != nil {
-		return err
-	}
-	properties, err := genV1ResourcesProperties(container.Cgroups, dbusConnection)
+	properties, err := genV1ResourcesProperties(container.Cgroups, m.dbus)
 	if err != nil {
 		return err
 	}
@@ -386,7 +375,7 @@ func (m *legacyManager) Set(container *configs.Config) error {
 		}
 	}
 
-	if err := dbusConnection.SetUnitProperties(getUnitName(container.Cgroups), true, properties...); err != nil {
+	if err := setUnitProperties(m.dbus, getUnitName(container.Cgroups), properties...); err != nil {
 		_ = m.Freeze(targetFreezerState)
 		return err
 	}
diff --git a/libcontainer/cgroups/systemd/v2.go b/libcontainer/cgroups/systemd/v2.go
index 70b5b368e..6703a63c8 100644
--- a/libcontainer/cgroups/systemd/v2.go
+++ b/libcontainer/cgroups/systemd/v2.go
@@ -26,6 +26,7 @@ type unifiedManager struct {
 	// path is like "/sys/fs/cgroup/user.slice/user-1001.slice/session-1.scope"
 	path     string
 	rootless bool
+	dbus     *dbusConnManager
 }
 
 func NewUnifiedManager(config *configs.Cgroup, path string, rootless bool) cgroups.Manager {
@@ -33,6 +34,7 @@ func NewUnifiedManager(config *configs.Cgroup, path string, rootless bool) cgrou
 		cgroups:  config,
 		path:     path,
 		rootless: rootless,
+		dbus:     newDbusConnManager(rootless),
 	}
 }
 
@@ -45,7 +47,7 @@ func NewUnifiedManager(config *configs.Cgroup, path string, rootless bool) cgrou
 // For the list of keys, see https://www.kernel.org/doc/Documentation/cgroup-v2.txt
 //
 // For the list of systemd unit properties, see systemd.resource-control(5).
-func unifiedResToSystemdProps(conn *systemdDbus.Conn, res map[string]string) (props []systemdDbus.Property, _ error) {
+func unifiedResToSystemdProps(cm *dbusConnManager, res map[string]string) (props []systemdDbus.Property, _ error) {
 	var err error
 
 	for k, v := range res {
@@ -83,7 +85,7 @@ func unifiedResToSystemdProps(conn *systemdDbus.Conn, res map[string]string) (pr
 					return nil, fmt.Errorf("unified resource %q quota value conversion error: %w", k, err)
 				}
 			}
-			addCpuQuota(conn, &props, quota, period)
+			addCpuQuota(cm, &props, quota, period)
 
 		case "cpu.weight":
 			num, err := strconv.ParseUint(v, 10, 64)
@@ -103,7 +105,7 @@ func unifiedResToSystemdProps(conn *systemdDbus.Conn, res map[string]string) (pr
 				"cpuset.mems": "AllowedMemoryNodes",
 			}
 			// systemd only supports these properties since v244
-			sdVer := systemdVersion(conn)
+			sdVer := systemdVersion(cm)
 			if sdVer >= 244 {
 				props = append(props,
 					newProp(m[k], bits))
@@ -163,7 +165,7 @@ func unifiedResToSystemdProps(conn *systemdDbus.Conn, res map[string]string) (pr
 	return props, nil
 }
 
-func genV2ResourcesProperties(c *configs.Cgroup, conn *systemdDbus.Conn) ([]systemdDbus.Property, error) {
+func genV2ResourcesProperties(c *configs.Cgroup, cm *dbusConnManager) ([]systemdDbus.Property, error) {
 	var properties []systemdDbus.Property
 	r := c.Resources
 
@@ -201,7 +203,7 @@ func genV2ResourcesProperties(c *configs.Cgroup, conn *systemdDbus.Conn) ([]syst
 			newProp("CPUWeight", r.CpuWeight))
 	}
 
-	addCpuQuota(conn, &properties, r.CpuQuota, r.CpuPeriod)
+	addCpuQuota(cm, &properties, r.CpuQuota, r.CpuPeriod)
 
 	if r.PidsLimit > 0 || r.PidsLimit == -1 {
 		properties = append(properties,
@@ -209,7 +211,7 @@ func genV2ResourcesProperties(c *configs.Cgroup, conn *systemdDbus.Conn) ([]syst
 			newProp("TasksMax", uint64(r.PidsLimit)))
 	}
 
-	err = addCpuset(conn, &properties, r.CpusetCpus, r.CpusetMems)
+	err = addCpuset(cm, &properties, r.CpusetCpus, r.CpusetMems)
 	if err != nil {
 		return nil, err
 	}
@@ -218,7 +220,7 @@ func genV2ResourcesProperties(c *configs.Cgroup, conn *systemdDbus.Conn) ([]syst
 
 	// convert Resources.Unified map to systemd properties
 	if r.Unified != nil {
-		unifiedProps, err := unifiedResToSystemdProps(conn, r.Unified)
+		unifiedProps, err := unifiedResToSystemdProps(cm, r.Unified)
 		if err != nil {
 			return nil, err
 		}
@@ -279,22 +281,18 @@ func (m *unifiedManager) Apply(pid int) error {
 	properties = append(properties,
 		newProp("DefaultDependencies", false))
 
-	dbusConnection, err := getDbusConnection(m.rootless)
-	if err != nil {
-		return err
-	}
-	resourcesProperties, err := genV2ResourcesProperties(c, dbusConnection)
+	resourcesProperties, err := genV2ResourcesProperties(c, m.dbus)
 	if err != nil {
 		return err
 	}
 	properties = append(properties, resourcesProperties...)
 	properties = append(properties, c.SystemdProps...)
 
-	if err := startUnit(dbusConnection, unitName, properties); err != nil {
+	if err := startUnit(m.dbus, unitName, properties); err != nil {
 		return errors.Wrapf(err, "error while starting unit %q with properties %+v", unitName, properties)
 	}
 
-	if err = m.initPath(); err != nil {
+	if err := m.initPath(); err != nil {
 		return err
 	}
 	if err := fs2.CreateCgroupPath(m.path, m.cgroups); err != nil {
@@ -310,17 +308,13 @@ func (m *unifiedManager) Destroy() error {
 	m.mu.Lock()
 	defer m.mu.Unlock()
 
-	dbusConnection, err := getDbusConnection(m.rootless)
-	if err != nil {
-		return err
-	}
 	unitName := getUnitName(m.cgroups)
-	if err := stopUnit(dbusConnection, unitName); err != nil {
+	if err := stopUnit(m.dbus, unitName); err != nil {
 		return err
 	}
 
 	// XXX this is probably not needed, systemd should handle it
-	err = os.Remove(m.path)
+	err := os.Remove(m.path)
 	if err != nil && !os.IsNotExist(err) {
 		return err
 	}
@@ -349,7 +343,7 @@ func (m *unifiedManager) getSliceFull() (string, error) {
 	}
 
 	if m.rootless {
-		dbusConnection, err := getDbusConnection(m.rootless)
+		dbusConnection, err := m.dbus.getConnection()
 		if err != nil {
 			return "", err
 		}
@@ -432,11 +426,7 @@ func (m *unifiedManager) GetStats() (*cgroups.Stats, error) {
 }
 
 func (m *unifiedManager) Set(container *configs.Config) error {
-	dbusConnection, err := getDbusConnection(m.rootless)
-	if err != nil {
-		return err
-	}
-	properties, err := genV2ResourcesProperties(m.cgroups, dbusConnection)
+	properties, err := genV2ResourcesProperties(m.cgroups, m.dbus)
 	if err != nil {
 		return err
 	}
@@ -464,7 +454,7 @@ func (m *unifiedManager) Set(container *configs.Config) error {
 		}
 	}
 
-	if err := dbusConnection.SetUnitProperties(getUnitName(m.cgroups), true, properties...); err != nil {
+	if err := setUnitProperties(m.dbus, getUnitName(m.cgroups), properties...); err != nil {
 		_ = m.Freeze(targetFreezerState)
 		return errors.Wrap(err, "error while setting unit properties")
 	}