diff --git a/templates/cluster-template-flatcar.yaml b/templates/cluster-template-flatcar.yaml
index 2978263dab6..d5b4255b7ea 100644
--- a/templates/cluster-template-flatcar.yaml
+++ b/templates/cluster-template-flatcar.yaml
@@ -91,6 +91,8 @@ spec:
                 contents: |
                   [Unit]
                   After=oem-cloudinit.service
+                  # kubeadm must run after containerd - see https://github.com/kubernetes-sigs/image-builder/issues/939.
+                  After=containerd.service
           # Workaround for https://github.com/kubernetes-sigs/cluster-api/issues/7679.
           storage:
             disks:
@@ -218,6 +220,8 @@ spec:
                   contents: |
                     [Unit]
                     After=oem-cloudinit.service
+                    # kubeadm must run after containerd - see https://github.com/kubernetes-sigs/image-builder/issues/939.
+                    After=containerd.service
       joinConfiguration:
         nodeRegistration:
           kubeletExtraArgs:
diff --git a/templates/flavors/flatcar/machine-deployment.yaml b/templates/flavors/flatcar/machine-deployment.yaml
index 59ccfde5794..da7ea9c889b 100644
--- a/templates/flavors/flatcar/machine-deployment.yaml
+++ b/templates/flavors/flatcar/machine-deployment.yaml
@@ -67,6 +67,8 @@ spec:
                   contents: |
                     [Unit]
                     After=oem-cloudinit.service
+                    # kubeadm must run after containerd - see https://github.com/kubernetes-sigs/image-builder/issues/939.
+                    After=containerd.service
       joinConfiguration:
         nodeRegistration:
           kubeletExtraArgs:
diff --git a/templates/flavors/flatcar/patches/kubeadm-controlplane.yaml b/templates/flavors/flatcar/patches/kubeadm-controlplane.yaml
index 4dad6e8d26b..b2a3efcbb9c 100644
--- a/templates/flavors/flatcar/patches/kubeadm-controlplane.yaml
+++ b/templates/flavors/flatcar/patches/kubeadm-controlplane.yaml
@@ -28,6 +28,8 @@ spec:
                 contents: |
                   [Unit]
                   After=oem-cloudinit.service
+                  # kubeadm must run after containerd - see https://github.com/kubernetes-sigs/image-builder/issues/939.
+                  After=containerd.service
           # Workaround for https://github.com/kubernetes-sigs/cluster-api/issues/7679.
           storage:
             disks:
diff --git a/templates/test/ci/cluster-template-prow-flatcar.yaml b/templates/test/ci/cluster-template-prow-flatcar.yaml
index 38a0c5ddf31..f59382116f5 100644
--- a/templates/test/ci/cluster-template-prow-flatcar.yaml
+++ b/templates/test/ci/cluster-template-prow-flatcar.yaml
@@ -96,6 +96,8 @@ spec:
                 contents: |
                   [Unit]
                   After=oem-cloudinit.service
+                  # kubeadm must run after containerd - see https://github.com/kubernetes-sigs/image-builder/issues/939.
+                  After=containerd.service
           # Workaround for https://github.com/kubernetes-sigs/cluster-api/issues/7679.
           storage:
             disks:
@@ -223,6 +225,8 @@ spec:
                   contents: |
                     [Unit]
                     After=oem-cloudinit.service
+                    # kubeadm must run after containerd - see https://github.com/kubernetes-sigs/image-builder/issues/939.
+                    After=containerd.service
       joinConfiguration:
         nodeRegistration:
           kubeletExtraArgs: