diff --git a/server/src/main/java/com/cloud/storage/VolumeApiServiceImpl.java b/server/src/main/java/com/cloud/storage/VolumeApiServiceImpl.java
index 9b2f4f831d3e..d5443662e23d 100644
--- a/server/src/main/java/com/cloud/storage/VolumeApiServiceImpl.java
+++ b/server/src/main/java/com/cloud/storage/VolumeApiServiceImpl.java
@@ -1524,13 +1524,26 @@ protected boolean isNotPossibleToResize(VolumeVO volume, DiskOfferingVO diskOffe
         return isOfferingEnforcingRootDiskSize && isRoot && isNotIso;
     }
 
-    private void checkIfVolumeIsRootAndVmIsRunning(Long newSize, VolumeVO volume, VMInstanceVO vmInstanceVO) {
-        if (!volume.getSize().equals(newSize) && volume.getVolumeType().equals(Volume.Type.ROOT) && !State.Stopped.equals(vmInstanceVO.getState())) {
-            throw new InvalidParameterValueException(String.format("Cannot resize ROOT volume [%s] when VM is not on Stopped State. VM %s is in state %s", volume.getName(), vmInstanceVO
+    protected void checkIfVolumeIsRootAndVmIsRunning(Long newSize, VolumeVO volume, VMInstanceVO vmInstanceVO) {
+        if (!volume.getSize().equals(newSize) && volume.getVolumeType().equals(Volume.Type.ROOT) && !State.Stopped.equals(vmInstanceVO.getState())
+                && !isGrowOfVolumeOnRunningKvmVm(newSize, volume, vmInstanceVO)) {
+            throw new InvalidParameterValueException(String.format("Cannot resize ROOT volume [%s] when VM is not on Stopped State. VM %s is in state %s. "
+                    + "Only growing the ROOT volume of a Running KVM user VM is allowed without stopping it.", volume.getName(), vmInstanceVO
                     .getInstanceName(), vmInstanceVO.getState()));
         }
     }
 
+    /**
+     * KVM grows the disk of a running user VM in place (virsh blockresize), and a size-only resizeVolume of a
+     * ROOT volume already does so. Growing it through a new disk offering is the same operation.
+     * Shrinking still requires the VM to be stopped. Only user VMs are let through, since the resize orchestration
+     * (orchestrateResizeVolume) only looks up the running VM and its host for user VMs.
+     */
+    private boolean isGrowOfVolumeOnRunningKvmVm(Long newSize, VolumeVO volume, VMInstanceVO vmInstanceVO) {
+        return HypervisorType.KVM.equals(vmInstanceVO.getHypervisorType()) && VirtualMachine.Type.User.equals(vmInstanceVO.getType())
+                && State.Running.equals(vmInstanceVO.getState()) && newSize != null && newSize > volume.getSize();
+    }
+
     private void validateIops(Long minIops, Long maxIops, Storage.StoragePoolType poolType) {
         if (poolType == Storage.StoragePoolType.PowerFlex) {
             // PowerFlex takes iopsLimit as input, skip minIops validation
diff --git a/server/src/test/java/com/cloud/storage/VolumeApiServiceImplTest.java b/server/src/test/java/com/cloud/storage/VolumeApiServiceImplTest.java
index b806eb4afe5c..4e60aeec2f80 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;
@@ -2504,4 +2505,59 @@ public void testResizeVolumeInternal_VMware_VMRunning_ShouldThrowStateGuardError
                     e.getMessage() != null && e.getMessage().contains("VM should be in"));
         }
     }
+
+    private VolumeVO mockRootVolumeOfSize(long size) {
+        VolumeVO volume = Mockito.mock(VolumeVO.class);
+        Mockito.when(volume.getSize()).thenReturn(size);
+        Mockito.when(volume.getVolumeType()).thenReturn(Volume.Type.ROOT);
+        return volume;
+    }
+
+    private VMInstanceVO mockVm(HypervisorType hypervisorType, State state) {
+        VMInstanceVO vm = Mockito.mock(VMInstanceVO.class);
+        Mockito.lenient().when(vm.getHypervisorType()).thenReturn(hypervisorType);
+        Mockito.lenient().when(vm.getType()).thenReturn(VirtualMachine.Type.User);
+        Mockito.when(vm.getState()).thenReturn(state);
+        return vm;
+    }
+
+    @Test
+    public void checkIfVolumeIsRootAndVmIsRunningAllowsGrowOnRunningKvmVm() {
+        volumeApiServiceImpl.checkIfVolumeIsRootAndVmIsRunning(20L << 30, mockRootVolumeOfSize(10L << 30), mockVm(HypervisorType.KVM, State.Running));
+    }
+
+    @Test(expected = InvalidParameterValueException.class)
+    public void checkIfVolumeIsRootAndVmIsRunningRefusesShrinkOnRunningKvmVm() {
+        volumeApiServiceImpl.checkIfVolumeIsRootAndVmIsRunning(5L << 30, mockRootVolumeOfSize(10L << 30), mockVm(HypervisorType.KVM, State.Running));
+    }
+
+    @Test(expected = InvalidParameterValueException.class)
+    public void checkIfVolumeIsRootAndVmIsRunningRefusesGrowOnRunningNonKvmVm() {
+        volumeApiServiceImpl.checkIfVolumeIsRootAndVmIsRunning(20L << 30, mockRootVolumeOfSize(10L << 30), mockVm(HypervisorType.VMware, State.Running));
+    }
+
+    @Test(expected = InvalidParameterValueException.class)
+    public void checkIfVolumeIsRootAndVmIsRunningRefusesGrowOnRunningKvmSystemVm() {
+        VMInstanceVO vm = mockVm(HypervisorType.KVM, State.Running);
+        Mockito.when(vm.getType()).thenReturn(VirtualMachine.Type.DomainRouter);
+        volumeApiServiceImpl.checkIfVolumeIsRootAndVmIsRunning(20L << 30, mockRootVolumeOfSize(10L << 30), vm);
+    }
+
+    @Test(expected = InvalidParameterValueException.class)
+    public void checkIfVolumeIsRootAndVmIsRunningRefusesGrowOnKvmVmNotRunning() {
+        volumeApiServiceImpl.checkIfVolumeIsRootAndVmIsRunning(20L << 30, mockRootVolumeOfSize(10L << 30), mockVm(HypervisorType.KVM, State.Migrating));
+    }
+
+    @Test
+    public void checkIfVolumeIsRootAndVmIsRunningAllowsResizeOnStoppedVm() {
+        volumeApiServiceImpl.checkIfVolumeIsRootAndVmIsRunning(5L << 30, mockRootVolumeOfSize(10L << 30), mockVm(HypervisorType.VMware, State.Stopped));
+    }
+
+    @Test
+    public void checkIfVolumeIsRootAndVmIsRunningIgnoresDataDisk() {
+        VolumeVO volume = Mockito.mock(VolumeVO.class);
+        Mockito.when(volume.getSize()).thenReturn(10L << 30);
+        Mockito.when(volume.getVolumeType()).thenReturn(Volume.Type.DATADISK);
+        volumeApiServiceImpl.checkIfVolumeIsRootAndVmIsRunning(5L << 30, volume, Mockito.mock(VMInstanceVO.class));
+    }
 }