diff --git a/pkg/apis/core/validation/validation.go b/pkg/apis/core/validation/validation.go
index 9e2868f683e..678a4452e00 100644
--- a/pkg/apis/core/validation/validation.go
+++ b/pkg/apis/core/validation/validation.go
@@ -5503,6 +5503,10 @@ func ValidatePodResize(newPod, oldPod *core.Pod, opts PodValidationOptions) fiel
 		allErrs = append(allErrs, field.Invalid(specPath, newPod.Status.QOSClass, "Pod QOS Class may not change as a result of resizing"))
 	}
 
+	if !isPodResizeRequestSupported(*oldPod) {
+		allErrs = append(allErrs, field.Forbidden(specPath, "Pod running on node without support for resize"))
+	}
+
 	// Ensure that only CPU and memory resources are mutable.
 	originalCPUMemPodSpec := *newPod.Spec.DeepCopy()
 	var newContainers []core.Container
@@ -5543,6 +5547,23 @@ func ValidatePodResize(newPod, oldPod *core.Pod, opts PodValidationOptions) fiel
 	return allErrs
 }
 
+// isPodResizeRequestSupported checks whether the pod is running on a node with InPlacePodVerticalScaling enabled.
+func isPodResizeRequestSupported(pod core.Pod) bool {
+	// TODO: Remove this after GA+3 releases of InPlacePodVerticalScaling
+	// This code handles the version skew as described in the KEP.
+	// For handling version skew we're only allowing to update the Pod's Resources
+	// if the Pod already has Pod.Status.ContainerStatuses[i].Resources. This means
+	// that the apiserver would only allow updates to Pods running on Nodes with
+	// the InPlacePodVerticalScaling feature gate enabled.
+	for _, c := range pod.Status.ContainerStatuses {
+		if c.State.Running != nil {
+			return c.Resources != nil
+		}
+	}
+	// No running containers. We cannot tell whether the node supports resize at this point, so we assume it does.
+	return true
+}
+
 // ValidatePodBinding tests if required fields in the pod binding are legal.
 func ValidatePodBinding(binding *core.Binding) field.ErrorList {
 	allErrs := field.ErrorList{}
diff --git a/pkg/apis/core/validation/validation_test.go b/pkg/apis/core/validation/validation_test.go
index e22078723a4..636da34b2b1 100644
--- a/pkg/apis/core/validation/validation_test.go
+++ b/pkg/apis/core/validation/validation_test.go
@@ -25203,6 +25203,74 @@ func TestValidatePodResize(t *testing.T) {
 			new:  mkPod(core.ResourceList{}, getResources("200m", "0", "1Gi", ""), podtest.SetOS(core.Windows)),
 			err:  "Forbidden: windows pods cannot be resized",
 		},
+		{
+			test: "Pod with nil Resource field in Status",
+			old: mkPod(core.ResourceList{}, getResources("100m", "0", "1Gi", ""), podtest.SetStatus(core.PodStatus{
+				ContainerStatuses: []core.ContainerStatus{{
+					ContainerID: "docker://numbers",
+					Image:       "nginx:alpine",
+					Name:        "main",
+					Ready:       true,
+					Started:     proto.Bool(true),
+					Resources:   nil,
+					State: core.ContainerState{
+						Running: &core.ContainerStateRunning{
+							StartedAt: metav1.NewTime(time.Now()),
+						},
+					},
+				}},
+			})),
+			new: mkPod(core.ResourceList{}, getResources("200m", "0", "1Gi", "")),
+			err: "Forbidden: Pod running on node without support for resize",
+		},
+		{
+			test: "Pod with non-nil Resources field in Status",
+			old: mkPod(core.ResourceList{}, getResources("100m", "0", "1Gi", ""), podtest.SetStatus(core.PodStatus{
+				ContainerStatuses: []core.ContainerStatus{{
+					ContainerID: "docker://numbers",
+					Image:       "nginx:alpine",
+					Name:        "main",
+					Ready:       true,
+					Started:     proto.Bool(true),
+					Resources:   &core.ResourceRequirements{},
+					State: core.ContainerState{
+						Running: &core.ContainerStateRunning{
+							StartedAt: metav1.NewTime(time.Now()),
+						},
+					},
+				}},
+			})),
+			new: mkPod(core.ResourceList{}, getResources("200m", "0", "1Gi", "")),
+			err: "",
+		},
+		{
+			test: "Pod without running containers",
+			old: mkPod(core.ResourceList{}, getResources("100m", "0", "1Gi", ""), podtest.SetStatus(core.PodStatus{
+				ContainerStatuses: []core.ContainerStatus{},
+			})),
+			new: mkPod(core.ResourceList{}, getResources("200m", "0", "1Gi", "")),
+			err: "",
+		},
+		{
+			test: "Pod with containers which are not running yet",
+			old: mkPod(core.ResourceList{}, getResources("100m", "0", "1Gi", ""), podtest.SetStatus(core.PodStatus{
+				ContainerStatuses: []core.ContainerStatus{{
+					ContainerID: "docker://numbers",
+					Image:       "nginx:alpine",
+					Name:        "main",
+					Ready:       true,
+					Started:     proto.Bool(true),
+					Resources:   &core.ResourceRequirements{},
+					State: core.ContainerState{
+						Waiting: &core.ContainerStateWaiting{
+							Reason: "PodInitializing",
+						},
+					},
+				}},
+			})),
+			new: mkPod(core.ResourceList{}, getResources("200m", "0", "1Gi", "")),
+			err: "",
+		},
 	}
 
 	for _, test := range tests {