diff --git a/server/src/main/java/com/cloud/storage/VolumeApiServiceImpl.java b/server/src/main/java/com/cloud/storage/VolumeApiServiceImpl.java
index 9b2f4f831d3e..384f9e6fe269 100644
--- a/server/src/main/java/com/cloud/storage/VolumeApiServiceImpl.java
+++ b/server/src/main/java/com/cloud/storage/VolumeApiServiceImpl.java
@@ -1481,6 +1481,22 @@ public VolumeVO resizeVolume(ResizeVolumeCmd cmd) throws ResourceAllocationExcep
         }
     }
 
+    /**
+     * The resize orchestration (orchestrateResizeVolume) only tells the hypervisor about a running user VM. For a
+     * system VM the volume is resized on the storage, but the running guest is not told and keeps seeing the old size
+     * until it next starts. So a system VM's volume can only be resized while the system VM is stopped.
+     */
+    protected void validateSystemVmIsStoppedForResize(VolumeVO volume) {
+        if (volume.getInstanceId() == null) {
+            return;
+        }
+        VMInstanceVO vm = _vmInstanceDao.findById(volume.getInstanceId());
+        if (vm != null && vm.getType().isUsedBySystem() && !State.Stopped.equals(vm.getState())) {
+            throw new InvalidParameterValueException(String.format("Cannot resize volume [%s] of system VM %s while it is in state %s. "
+                    + "Stop the system VM before resizing its volume.", volume.getName(), vm.getInstanceName(), vm.getState()));
+        }
+    }
+
     protected void validateNoVmSnapshots(VolumeVO volume) {
         if (volume.getInstanceId() != null) {
             if (vmHasVmSnapshotsExceptKvmDiskOnlySnapshots(volume.getInstanceId())) {
@@ -2496,6 +2512,7 @@ private void validateVolumeResizeWithSize(VolumeVO volume, long currentSize, Lon
         // if the caller is looking to change the size of the volume
         if (newSize != null && currentSize != newSize) {
             validateNoVmSnapshots(volume);
+            validateSystemVmIsStoppedForResize(volume);
 
             if (!validateVolumeSizeInBytes(newSize)) {
                 throw new InvalidParameterValueException("Requested size out of range");
diff --git a/server/src/test/java/com/cloud/storage/VolumeApiServiceImplTest.java b/server/src/test/java/com/cloud/storage/VolumeApiServiceImplTest.java
index b806eb4afe5c..30810f68e238 100644
--- a/server/src/test/java/com/cloud/storage/VolumeApiServiceImplTest.java
+++ b/server/src/test/java/com/cloud/storage/VolumeApiServiceImplTest.java
@@ -139,6 +139,7 @@
 import com.cloud.vm.DiskProfile;
 import com.cloud.vm.UserVmManager;
 import com.cloud.vm.UserVmVO;
+import com.cloud.vm.VMInstanceVO;
 import com.cloud.vm.VirtualMachine;
 import com.cloud.vm.VirtualMachine.State;
 import com.cloud.vm.VirtualMachineManager;
@@ -2267,6 +2268,78 @@ public void validateNoVmSnapshotsTestVmHasVmSnapshotsExceptKvmDiskOnlySnapshotsI
         volumeApiServiceImpl.validateNoVmSnapshots(volumeVoMock);
     }
 
+    private VMInstanceVO mockVmInstance(VirtualMachine.Type type, State state) {
+        VMInstanceVO vm = Mockito.mock(VMInstanceVO.class);
+        Mockito.when(vm.getType()).thenReturn(type);
+        Mockito.lenient().when(vm.getState()).thenReturn(state);
+        Mockito.when(volumeVoMock.getInstanceId()).thenReturn(vmInstanceMockId);
+        Mockito.when(_vmInstanceDao.findById(vmInstanceMockId)).thenReturn(vm);
+        return vm;
+    }
+
+    @Test
+    public void validateSystemVmIsStoppedForResizeTestDetachedVolume() {
+        Mockito.when(volumeVoMock.getInstanceId()).thenReturn(null);
+
+        volumeApiServiceImpl.validateSystemVmIsStoppedForResize(volumeVoMock);
+
+        Mockito.verify(_vmInstanceDao, Mockito.never()).findById(Mockito.anyLong());
+    }
+
+    @Test
+    public void validateSystemVmIsStoppedForResizeTestRunningUserVm() {
+        mockVmInstance(VirtualMachine.Type.User, State.Running);
+
+        volumeApiServiceImpl.validateSystemVmIsStoppedForResize(volumeVoMock);
+    }
+
+    @Test
+    public void validateSystemVmIsStoppedForResizeTestStoppedRouter() {
+        mockVmInstance(VirtualMachine.Type.DomainRouter, State.Stopped);
+
+        volumeApiServiceImpl.validateSystemVmIsStoppedForResize(volumeVoMock);
+    }
+
+    @Test
+    public void validateSystemVmIsStoppedForResizeTestNotStoppedSystemVms() {
+        for (VirtualMachine.Type type : List.of(VirtualMachine.Type.DomainRouter, VirtualMachine.Type.ConsoleProxy,
+                VirtualMachine.Type.SecondaryStorageVm, VirtualMachine.Type.InternalLoadBalancerVm)) {
+            for (State state : List.of(State.Running, State.Starting, State.Stopping, State.Migrating)) {
+                mockVmInstance(type, state);
+                try {
+                    volumeApiServiceImpl.validateSystemVmIsStoppedForResize(volumeVoMock);
+                    Assert.fail("Resizing the volume of a " + type + " in state " + state + " must be refused");
+                } catch (InvalidParameterValueException e) {
+                    Assert.assertTrue(e.getMessage(), e.getMessage().contains("Stop the system VM"));
+                }
+            }
+        }
+    }
+
+    @Test
+    public void resizeVolumeSizeOnlyOnRunningRouterIsRefused() throws ResourceAllocationException {
+        ResizeVolumeCmd cmd = new ResizeVolumeCmd();
+        ReflectionTestUtils.setField(cmd, "id", volumeMockId);
+        ReflectionTestUtils.setField(cmd, "size", 1000L); // GiB, a grow of the 425 GiB volumeVoMock
+
+        Mockito.when(volumeDaoMock.findById(volumeMockId)).thenReturn(volumeVoMock);
+        Mockito.when(volumeDaoMock.getHypervisorType(volumeMockId)).thenReturn(HypervisorType.KVM);
+        Mockito.when(volumeVoMock.getState()).thenReturn(Volume.State.Ready);
+        Mockito.when(volumeVoMock.getDiskOfferingId()).thenReturn(diskOfferingMockId);
+        Mockito.when(_diskOfferingDao.findById(diskOfferingMockId)).thenReturn(diskOfferingMock);
+        Mockito.doReturn(false).when(volumeApiServiceImpl).isNotPossibleToResize(volumeVoMock, diskOfferingMock);
+        Mockito.when(volumeDataFactoryMock.getVolume(volumeMockId)).thenReturn(volumeInfoMock);
+        mockVmInstance(VirtualMachine.Type.DomainRouter, State.Running);
+
+        try {
+            volumeApiServiceImpl.resizeVolume(cmd);
+            Assert.fail("A size-only resize of a running router's volume must be refused");
+        } catch (InvalidParameterValueException e) {
+            Assert.assertTrue(e.getMessage(), e.getMessage().contains("Stop the system VM"));
+        }
+        Mockito.verify(volumeServiceMock, Mockito.never()).resize(any(VolumeInfo.class));
+    }
+
     @Test
     public void vmHasVmSnapshotsExceptKvmDiskOnlySnapshotsTestMultipleDiskAndMemory () {
         List<VMSnapshotVO> snapList = generateVmSnapshotVoList(VMSnapshot.Type.DiskAndMemory, VMSnapshot.Type.DiskAndMemory);