diff --git a/backend/manager/modules/bll/src/main/java/org/ovirt/engine/core/bll/RunVmCommand.java b/backend/manager/modules/bll/src/main/java/org/ovirt/engine/core/bll/RunVmCommand.java
index 8aacfc87008..17c3185e350 100644
--- a/backend/manager/modules/bll/src/main/java/org/ovirt/engine/core/bll/RunVmCommand.java
+++ b/backend/manager/modules/bll/src/main/java/org/ovirt/engine/core/bll/RunVmCommand.java
@@ -1078,8 +1078,13 @@ protected boolean validateImpl() {
             return false;
         }
 
-        if (getVm().getCustomCompatibilityVersion() != null &&
-                vm.getCustomCompatibilityVersion().less(getStoragePool().getCompatibilityVersion())) {
+        // Skip the compatibility version check when resuming a Paused or Suspended VM,
+        // since the VM was already running with its custom compatibility version before
+        // the data center was upgraded and is only being resumed, not started fresh.
+        if (vm.getCustomCompatibilityVersion() != null &&
+                vm.getCustomCompatibilityVersion().less(getStoragePool().getCompatibilityVersion()) &&
+                vm.getStatus() != VMStatus.Paused &&
+                vm.getStatus() != VMStatus.Suspended) {
             return failValidation(EngineMessage.ACTION_TYPE_FAILED_VM_COMPATIBILITY_VERSION_NOT_SUPPORTED,
                     String.format("$VmName %1$s", getVm().getName()),
                     String.format("$VmVersion %1$s", getVm().getCustomCompatibilityVersion().toString()),
diff --git a/backend/manager/modules/bll/src/test/java/org/ovirt/engine/core/bll/RunVmCommandTest.java b/backend/manager/modules/bll/src/test/java/org/ovirt/engine/core/bll/RunVmCommandTest.java
index 5d17e6ffb89..ea28c0a7eb8 100644
--- a/backend/manager/modules/bll/src/test/java/org/ovirt/engine/core/bll/RunVmCommandTest.java
+++ b/backend/manager/modules/bll/src/test/java/org/ovirt/engine/core/bll/RunVmCommandTest.java
@@ -44,6 +44,7 @@
 import org.mockito.junit.jupiter.MockitoSettings;
 import org.mockito.quality.Strictness;
 import org.ovirt.engine.core.bll.context.CommandContext;
+import org.ovirt.engine.core.bll.interfaces.BackendInternal;
 import org.ovirt.engine.core.bll.network.host.NetworkDeviceHelper;
 import org.ovirt.engine.core.bll.network.host.VfScheduler;
 import org.ovirt.engine.core.bll.scheduling.SchedulingManager;
@@ -70,6 +71,8 @@
 import org.ovirt.engine.core.common.businessentities.storage.StorageType;
 import org.ovirt.engine.core.common.config.ConfigValues;
 import org.ovirt.engine.core.common.errors.EngineException;
+import org.ovirt.engine.core.common.errors.EngineMessage;
+import org.ovirt.engine.core.common.interfaces.ErrorTranslator;
 import org.ovirt.engine.core.common.interfaces.VDSBrokerFrontend;
 import org.ovirt.engine.core.common.osinfo.OsRepository;
 import org.ovirt.engine.core.common.utils.VmDeviceType;
@@ -78,6 +81,7 @@
 import org.ovirt.engine.core.common.vdscommands.VDSReturnValue;
 import org.ovirt.engine.core.compat.Guid;
 import org.ovirt.engine.core.compat.Version;
+import org.ovirt.engine.core.dal.dbbroker.auditloghandling.AuditLogDirector;
 import org.ovirt.engine.core.dao.DiskImageDao;
 import org.ovirt.engine.core.dao.SnapshotDao;
 import org.ovirt.engine.core.dao.StorageServerConnectionDao;
@@ -159,6 +163,12 @@ public class RunVmCommandTest extends BaseCommandTest {
     @Mock
     private ResourceManager resourceManager;
 
+    @Mock
+    private BackendInternal backend;
+
+    @Mock
+    private AuditLogDirector auditLogDirector;
+
     private static final String ACTIVE_ISO_PREFIX =
             "/rhev/data-center/mnt/some_computer/f6bccab4-e2f5-4e02-bba0-5748a7bc07b6/images/11111111-1111-1111-1111-111111111111";
     private static final String INACTIVE_ISO_PREFIX = "";
@@ -376,6 +386,7 @@ public void setUp() {
         doNothing().when(command).initParametersForExternalNetworks(null, false);
         doReturn(Collections.emptyMap()).when(command).flushPassthroughVnicToVfMap();
         doReturn(vmManager).when(command).getVmManager();
+        when(backend.getErrorsTranslator()).thenReturn(mock(ErrorTranslator.class));
         mockBackend();
     }
 
@@ -402,6 +413,73 @@ public void testValidate() {
         ValidateTestUtils.runAndAssertValidateSuccess(command);
     }
 
+    @Test
+    @MockedConfig("mockConfiguration")
+    public void testValidateFailsOnOlderCustomCompatibilityVersionWhenVmDown() {
+        final VM vm = new VM();
+        vm.setStatus(VMStatus.Down);
+        vm.setCustomCompatibilityVersion(new Version(4, 7));
+        command.setVm(vm);
+        StoragePool storagePool = new StoragePool();
+        storagePool.setCompatibilityVersion(new Version(4, 8));
+        command.setStoragePool(storagePool);
+        doReturn(true).when(command).checkRngDeviceClusterCompatibility();
+        doReturn(true).when(command).checkPayload(any());
+        doReturn(ValidationResult.VALID).when(command).checkDisksInBackupStorage();
+        doReturn(false).when(command).isVmDuringBackup();
+        doNothing().when(command).checkVmLeaseStorageDomain();
+        Cluster cluster = new Cluster();
+        cluster.setArchitecture(ArchitectureType.x86_64);
+        cluster.setCompatibilityVersion(new Version(4, 8));
+        command.setCluster(cluster);
+        ValidateTestUtils.runAndAssertValidateFailure(command,
+                EngineMessage.ACTION_TYPE_FAILED_VM_COMPATIBILITY_VERSION_NOT_SUPPORTED);
+    }
+
+    @Test
+    @MockedConfig("mockConfiguration")
+    public void testValidateSucceedsOnOlderCustomCompatibilityVersionWhenVmSuspended() {
+        final VM vm = new VM();
+        vm.setStatus(VMStatus.Suspended);
+        vm.setCustomCompatibilityVersion(new Version(4, 7));
+        command.setVm(vm);
+        StoragePool storagePool = new StoragePool();
+        storagePool.setCompatibilityVersion(new Version(4, 8));
+        command.setStoragePool(storagePool);
+        doReturn(true).when(command).checkRngDeviceClusterCompatibility();
+        doReturn(true).when(command).checkPayload(any());
+        doReturn(ValidationResult.VALID).when(command).checkDisksInBackupStorage();
+        doReturn(false).when(command).isVmDuringBackup();
+        doNothing().when(command).checkVmLeaseStorageDomain();
+        Cluster cluster = new Cluster();
+        cluster.setArchitecture(ArchitectureType.x86_64);
+        cluster.setCompatibilityVersion(new Version(4, 8));
+        command.setCluster(cluster);
+        ValidateTestUtils.runAndAssertValidateSuccess(command);
+    }
+
+    @Test
+    @MockedConfig("mockConfiguration")
+    public void testValidateSucceedsOnOlderCustomCompatibilityVersionWhenVmPaused() {
+        final VM vm = new VM();
+        vm.setStatus(VMStatus.Paused);
+        vm.setCustomCompatibilityVersion(new Version(4, 7));
+        command.setVm(vm);
+        StoragePool storagePool = new StoragePool();
+        storagePool.setCompatibilityVersion(new Version(4, 8));
+        command.setStoragePool(storagePool);
+        doReturn(true).when(command).checkRngDeviceClusterCompatibility();
+        doReturn(true).when(command).checkPayload(any());
+        doReturn(ValidationResult.VALID).when(command).checkDisksInBackupStorage();
+        doReturn(false).when(command).isVmDuringBackup();
+        doNothing().when(command).checkVmLeaseStorageDomain();
+        Cluster cluster = new Cluster();
+        cluster.setArchitecture(ArchitectureType.x86_64);
+        cluster.setCompatibilityVersion(new Version(4, 8));
+        command.setCluster(cluster);
+        ValidateTestUtils.runAndAssertValidateSuccess(command);
+    }
+
     public static Stream<Arguments> validateUnsupportedRng() {
         Set<VmRngDevice.Source> sourcesEmpty = new HashSet<>();
         Set<VmRngDevice.Source> sourcesRandom = new HashSet<>();