diff --git a/test/assets/ipv6-network.xml b/test/assets/ipv6-network.xml
index bce8224ef1..6de995e742 100644
--- a/test/assets/ipv6-network.xml
+++ b/test/assets/ipv6-network.xml
@@ -1,6 +1,10 @@
 <network>
   <name>${VM_IPV6_NETWORK}</name>
-  <forward mode='none'/>
+  <forward mode="nat">
+    <nat ipv6='yes'>
+      <port start='1024' end='65535'/>
+    </nat>
+  </forward>
   <ip family="ipv6" address="2001:db8:ca7:ff::1" prefix="96">
     <dhcp>
       <range start="2001:db8:ca7:ff::1000" end="2001:db8:ca7:ff::2000" />
diff --git a/test/bin/scenario.sh b/test/bin/scenario.sh
index 9e2fe9c59a..684b657062 100755
--- a/test/bin/scenario.sh
+++ b/test/bin/scenario.sh
@@ -257,6 +257,7 @@ prepare_kickstart() {
             -e "s|REPLACE_FIPS_ENABLED|${fips_enabled}|g" \
             -e "s|REPLACE_ENABLE_MIRROR|${ENABLE_REGISTRY_MIRROR}|g" \
             -e "s|REPLACE_MIRROR_HOSTNAME|${hostname}|g" \
+            -e "s|REPLACE_VM_BRIDGE_IP|${VM_BRIDGE_IP}|g" \
             "${ifile}" > "${output_file}"
     done
     record_junit "${vmname}" "prepare_kickstart" "OK"
diff --git a/test/kickstart-templates/includes/post-containers.cfg b/test/kickstart-templates/includes/post-containers.cfg
index 7b20a7538c..80e582529e 100644
--- a/test/kickstart-templates/includes/post-containers.cfg
+++ b/test/kickstart-templates/includes/post-containers.cfg
@@ -8,6 +8,8 @@ chmod 600 /etc/crio/openshift-pull-secret
 
 if REPLACE_ENABLE_MIRROR; then
     # Setup mirror registries configuration here, as the hostname is dynamic and the file is verbose.
+    # Use hostnames as IP addresses are not allowed. Since ec2 hostnames do not resolve to IPv6 addresses
+    # the /etc/hosts file will contain the hostname with the bridge IP from the host.
     mkdir -p /etc/containers/registries.conf.d
     cat > /etc/containers/registries.conf.d/999-microshift-mirror.conf <<EOF
 [[registry]]
@@ -51,4 +53,8 @@ EOF
         }
 }
 EOF
+
+cat >> /etc/hosts <<EOF
+REPLACE_VM_BRIDGE_IP REPLACE_MIRROR_HOSTNAME
+EOF
 fi
diff --git a/test/resources/kubeconfig.resource b/test/resources/kubeconfig.resource
index 9d89b958a9..5930b7bc9c 100644
--- a/test/resources/kubeconfig.resource
+++ b/test/resources/kubeconfig.resource
@@ -4,6 +4,7 @@ Documentation       Keywords for accessing a kubeconfig file for the MicroShift
 Library             OperatingSystem
 Library             String
 Library             DataFormats.py
+Library             libipv6.py
 Resource            ../resources/microshift-host.resource
 Resource            ../resources/common.resource
 
@@ -31,9 +32,10 @@ Setup Kubeconfig
     # If we have been given an explicit API port to use, make sure that
     # port appears in the kubeconfig file.
     IF    "${API_PORT}"!="${EMPTY}"
+        ${ip}=    Add Brackets If Ipv6    ${USHIFT_HOST}
         ${kubeconfig}=    Update Kubeconfig Server Url
         ...    ${kubeconfig}
-        ...    https://${USHIFT_HOST}:${API_PORT}
+        ...    https://${ip}:${API_PORT}
     END
     ${path}=    Create Random Temp File    ${kubeconfig}
     Set Suite Variable    \${KUBECONFIG}    ${path}
diff --git a/test/resources/microshift-network.resource b/test/resources/microshift-network.resource
index 72c0bdfb5e..0f5770cc97 100644
--- a/test/resources/microshift-network.resource
+++ b/test/resources/microshift-network.resource
@@ -47,11 +47,12 @@ Access Hello Microshift
     ...    ${ushift_ip}=${USHIFT_HOST}
     ...    ${path}=${EMPTY}
     ...    ${scheme}=http
+    ...    ${hostname}=hello-microshift.cluster.local
 
     ${ip}=    Add Brackets If Ipv6    ${ushift_ip}
 
-    ${connect_to}=    Set Variable    "hello-microshift.cluster.local::${ip}:"
-    ${url_path}=    Set Variable    "${scheme}://hello-microshift.cluster.local:${ushift_port}${path}"
+    ${connect_to}=    Set Variable    "${hostname}::${ip}:"
+    ${url_path}=    Set Variable    "${scheme}://${hostname}:${ushift_port}${path}"
 
     ${result}=    Run Process
     ...    curl -k -i ${url_path} --connect-to ${connect_to}
@@ -61,26 +62,38 @@ Access Hello Microshift
 
 Access Hello MicroShift Success
     [Documentation]    Expect 200 OK when accessing "hello microshift" through the router.
-    [Arguments]    ${ushift_port}    ${ushift_ip}=${USHIFT_HOST}    ${path}=${EMPTY}    ${scheme}=http
+    [Arguments]
+    ...    ${ushift_port}
+    ...    ${ushift_ip}=${USHIFT_HOST}
+    ...    ${path}=${EMPTY}
+    ...    ${scheme}=http
+    ...    ${hostname}=hello-microshift.cluster.local
 
     ${rc}    ${stdout}    ${stderr}=    Access Hello MicroShift
     ...    ushift_port=${ushift_port}
     ...    ushift_ip=${ushift_ip}
     ...    path=${path}
     ...    scheme=${scheme}
+    ...    hostname=${hostname}
     Should Be Equal As Integers    ${rc}    0
     Should Match Regexp    ${stdout}    HTTP.*200
     Should Match    ${stdout}    *Hello MicroShift*
 
 Access Hello MicroShift No Route
     [Documentation]    Expect 503 Service Unavailable when accessing "hello microshift" through the router.
-    [Arguments]    ${ushift_port}    ${ushift_ip}=${USHIFT_HOST}    ${path}=${EMPTY}    ${scheme}=http
+    [Arguments]
+    ...    ${ushift_port}
+    ...    ${ushift_ip}=${USHIFT_HOST}
+    ...    ${path}=${EMPTY}
+    ...    ${scheme}=http
+    ...    ${hostname}=hello-microshift.cluster.local
 
     ${rc}    ${stdout}    ${stderr}=    Access Hello MicroShift
     ...    ushift_port=${ushift_port}
     ...    ushift_ip=${ushift_ip}
     ...    path=${path}
     ...    scheme=${scheme}
+    ...    hostname=${hostname}
     Should Be Equal As Integers    ${rc}    0
     Should Match Regexp    ${stdout}    HTTP.*503
 
diff --git a/test/scenarios/el94-src@ipv6.sh b/test/scenarios/el94-src@ipv6.sh
new file mode 100644
index 0000000000..92fd6336b0
--- /dev/null
+++ b/test/scenarios/el94-src@ipv6.sh
@@ -0,0 +1,28 @@
+#!/bin/bash
+
+# Sourced from scenario.sh and uses functions defined there.
+
+# Redefine network-related settings to use the dedicated network bridge
+# shellcheck disable=SC2034  # used elsewhere
+VM_BRIDGE_IP="$(get_vm_bridge_ip "${VM_IPV6_NETWORK}")"
+# shellcheck disable=SC2034  # used elsewhere
+WEB_SERVER_URL="http://[${VM_BRIDGE_IP}]:${WEB_SERVER_PORT}"
+# shellcheck disable=SC2034  # used elsewhere
+BOOTC_REGISTRY_URL="${VM_BRIDGE_IP}:5000"
+# Redefine registry mirror. The redhat.registry.io does not resolve to
+# ipv6 and the mirror is mandatory.
+# shellcheck disable=SC2034  # used elsewhere
+ENABLE_REGISTRY_MIRROR=true
+
+scenario_create_vms() {
+    prepare_kickstart host1 kickstart.ks.template rhel-9.4-microshift-source
+    launch_vm host1 rhel-9.4 "${VM_IPV6_NETWORK}"
+}
+
+scenario_remove_vms() {
+    remove_vm host1
+}
+
+scenario_run_tests() {
+    run_tests host1 suites/ipv6/singlestack.robot
+}
diff --git a/test/suites/ipv6/singlestack.robot b/test/suites/ipv6/singlestack.robot
new file mode 100644
index 0000000000..2df82bf460
--- /dev/null
+++ b/test/suites/ipv6/singlestack.robot
@@ -0,0 +1,104 @@
+*** Settings ***
+Documentation       Tests related to MicroShift running in an IPv6-only host
+
+Resource            ../../resources/common.resource
+Resource            ../../resources/oc.resource
+Resource            ../../resources/ostree-health.resource
+Resource            ../../resources/microshift-network.resource
+Library             ../../resources/libipv6.py
+
+Suite Setup         Setup
+Suite Teardown      Teardown
+
+Test Tags           ipv6    network
+
+
+*** Variables ***
+${USHIFT_HOST}      ${EMPTY}
+${HOSTNAME}         hello-microshift.ipv6.cluster.local
+
+
+*** Test Cases ***
+Verify Router Serves IPv6
+    [Documentation]    Verify router is capable of serving ipv6 traffic.
+    [Setup]    Run Keywords
+    ...    Create Hello MicroShift Pod
+    ...    Expose Hello MicroShift Service Via Route
+    ...    Restart Router
+
+    Must Be Ipv6    ${USHIFT_HOST}
+    Wait Until Keyword Succeeds    10x    6s
+    ...    Access Hello Microshift Success    ushift_port=${HTTP_PORT}    hostname=${HOSTNAME}
+
+    DNS Entry For Route Should Resolve
+
+    [Teardown]    Run Keywords
+    ...    Delete Hello MicroShift Route
+    ...    Delete Hello MicroShift Pod And Service
+    ...    Wait For Service Deletion With Timeout
+
+Verify All Services Are Ipv6
+    [Documentation]    Check all services are running IPv6 only
+
+    All Services Are Ipv6
+
+
+*** Keywords ***
+Setup
+    [Documentation]    Test suite setup
+    Login MicroShift Host
+    Setup Suite With Namespace
+    Wait Until Greenboot Health Check Exited
+
+Teardown
+    [Documentation]    Test suite teardown
+    Logout MicroShift Host
+
+Delete Hello MicroShift Route
+    [Documentation]    Delete route for cleanup.
+    Oc Delete    route/hello-microshift -n ${NAMESPACE}
+
+Wait For Service Deletion With Timeout
+    [Documentation]    Polls for service and endpoint by "app=hello-microshift" label. Fails if timeout
+    ...    expires. This check is unique to this test suite because each test here reuses the same namespace. Since
+    ...    the tests reuse the service name, a small race window exists between the teardown of one test and the setup
+    ...    of the next. This produces flakey failures when the service or endpoint names collide.
+    Wait Until Keyword Succeeds    30s    1s
+    ...    Network APIs With Test Label Are Gone
+
+Expose Hello MicroShift Service Via Route
+    [Documentation]    Expose the "hello microshift" application through the Route
+    Oc Expose    pod hello-microshift -n ${NAMESPACE}
+    Oc Expose    svc hello-microshift --hostname ${HOSTNAME} -n ${NAMESPACE}
+
+Network APIs With Test Label Are Gone
+    [Documentation]    Check for service and endpoint by "app=hello-microshift" label. Succeeds if response matches
+    ...    "No resources found in <namespace> namespace." Fail if not.
+    ${match_string}=    Catenate    No resources found in    ${NAMESPACE}    namespace.
+    ${match_string}=    Remove String    ${match_string}    "
+    ${response}=    Run With Kubeconfig    oc get svc,ep -l app\=hello-microshift -n ${NAMESPACE}
+    Should Be Equal As Strings    ${match_string}    ${response}    strip_spaces=True
+
+DNS Entry For Route Should Resolve
+    [Documentation]    Resolve hello-microshift route via mDNS from the hypervisor/RF runner.
+    ...    Expects RF runner host has opened port 5353 for libvirt zone.
+
+    ${result}=    Run Process
+    ...    avahi-resolve-host-name ${HOSTNAME}
+    ...    shell=True
+    ...    timeout=15s
+    Should Be Equal As Integers    0    ${result.rc}
+    Log Many    ${result.stdout}    ${result.stderr}
+    @{words}=    Split String    ${result.stdout}
+    Must Be Ipv6    ${words}[1]
+
+Restart Router
+    [Documentation]    Restart the router and wait for readiness again. The router is sensitive to apiserver
+    ...    downtime and might need a restart (after the apiserver is ready) to resync all the routes.
+    Run With Kubeconfig    oc rollout restart deployment router-default -n openshift-ingress
+    Named Deployment Should Be Available    router-default    openshift-ingress    5m
+
+All Services Are Ipv6
+    [Documentation]    Retrieve all services and check none of them have an IPv4 family
+    ${response}=    Run With Kubeconfig    oc get svc -A -o jsonpath='{.items[*].spec.ipFamilies[*]}'
+    Should Not Contain    ${response}    IPv4