diff --git a/pkg/kubelet/kubelet_getters.go b/pkg/kubelet/kubelet_getters.go
index 491ce594dd3..b51adf24174 100644
--- a/pkg/kubelet/kubelet_getters.go
+++ b/pkg/kubelet/kubelet_getters.go
@@ -120,8 +120,9 @@ func (kl *Kubelet) ListPodsFromDisk() ([]types.UID, error) {
 // user namespaces.
 func (kl *Kubelet) HandlerSupportsUserNamespaces(rtHandler string) (bool, error) {
 	rtHandlers := kl.runtimeState.runtimeHandlers()
-	if rtHandlers == nil {
-		return false, fmt.Errorf("runtime handlers are not set")
+	if len(rtHandlers) == 0 {
+		// The slice is empty if the runtime is old and doesn't support this message.
+		return false, nil
 	}
 	for _, h := range rtHandlers {
 		if h.Name == rtHandler {
diff --git a/pkg/kubelet/userns/userns_manager.go b/pkg/kubelet/userns/userns_manager.go
index 57d38b972df..728757b4f19 100644
--- a/pkg/kubelet/userns/userns_manager.go
+++ b/pkg/kubelet/userns/userns_manager.go
@@ -417,10 +417,15 @@ func (m *UsernsManager) GetOrCreateUserNamespaceMappings(pod *v1.Pod, runtimeHan
 	// From here onwards, hostUsers=false and the feature gate is enabled.
 
 	// if the pod requested a user namespace and the runtime doesn't support user namespaces then return an error.
-	if handlerSupportsUserns, err := m.kl.HandlerSupportsUserNamespaces(runtimeHandler); err != nil {
-		return nil, err
-	} else if !handlerSupportsUserns {
-		return nil, fmt.Errorf("RuntimeClass handler %q does not support user namespaces", runtimeHandler)
+	if handlerSupportsUserns, err := m.kl.HandlerSupportsUserNamespaces(runtimeHandler); err != nil || !handlerSupportsUserns {
+		msg := "can't set `spec.hostUsers: false`, runtime does not support user namespaces"
+		if runtimeHandler != "" {
+			msg = fmt.Sprintf("can't set `spec.hostUsers: false`, RuntimeClass handler %q does not support user namespaces", runtimeHandler)
+		}
+		if err != nil {
+			return nil, fmt.Errorf("%v: %w", msg, err)
+		}
+		return nil, fmt.Errorf("%v", msg)
 	}
 
 	m.lock.Lock()
@@ -435,12 +440,12 @@ func (m *UsernsManager) GetOrCreateUserNamespaceMappings(pod *v1.Pod, runtimeHan
 	if string(content) != "" {
 		userNs, err = m.parseUserNsFileAndRecord(pod.UID, content)
 		if err != nil {
-			return nil, err
+			return nil, fmt.Errorf("user namespace: %w", err)
 		}
 	} else {
 		userNs, err = m.createUserNs(pod)
 		if err != nil {
-			return nil, err
+			return nil, fmt.Errorf("create user namespace: %w", err)
 		}
 	}
 
@@ -491,7 +496,7 @@ func (m *UsernsManager) CleanupOrphanedPodUsernsAllocations(pods []*v1.Pod, runn
 	allFound := sets.New[string]()
 	found, err := m.kl.ListPodsFromDisk()
 	if err != nil {
-		return err
+		return fmt.Errorf("user namespace: read pods from disk: %w", err)
 	}
 
 	for _, podUID := range found {