diff --git a/flow-server/src/main/java/com/vaadin/flow/router/internal/DefaultRouteResolver.java b/flow-server/src/main/java/com/vaadin/flow/router/internal/DefaultRouteResolver.java
index cfd7c2e7885..63944c2a540 100644
--- a/flow-server/src/main/java/com/vaadin/flow/router/internal/DefaultRouteResolver.java
+++ b/flow-server/src/main/java/com/vaadin/flow/router/internal/DefaultRouteResolver.java
@@ -25,6 +25,7 @@
 import com.vaadin.flow.router.NavigationStateBuilder;
 import com.vaadin.flow.router.NotFoundException;
 import com.vaadin.flow.router.RouteResolver;
+import com.vaadin.flow.router.RouterLayout;
 import com.vaadin.flow.server.RouteRegistry;
 import com.vaadin.flow.internal.menu.MenuRegistry;
 import com.vaadin.flow.server.menu.AvailableViewInfo;
@@ -58,15 +59,16 @@ public NavigationState resolve(ResolveRequest request) {
                                         : "/" + clientPath);
                 if (viewInfo != null && viewInfo.flowLayout()) {
 
-                    Class<? extends Component> layout = (Class<? extends Component>) registry
+                    Class<? extends RouterLayout> layout = registry
                             .getLayout(path);
                     if (layout == null) {
                         throw new NotFoundException(
                                 "No layout for client path '%s'"
                                         .formatted(path));
                     }
-                    RouteTarget target = new RouteTarget(layout,
-                            Collections.emptyList());
+                    RouteTarget target = new RouteTarget(
+                            (Class<? extends Component>) layout, RouteUtil
+                                    .getParentLayoutsForNonRouteTarget(layout));
                     navigationResult = new NavigationRouteTarget(
                             navigationResult.getPath(), target,
                             Collections.emptyMap());
diff --git a/flow-server/src/test/java/com/vaadin/flow/router/DefaultRouteResolverTest.java b/flow-server/src/test/java/com/vaadin/flow/router/DefaultRouteResolverTest.java
index 999a7dc4fe1..8c576e535be 100644
--- a/flow-server/src/test/java/com/vaadin/flow/router/DefaultRouteResolverTest.java
+++ b/flow-server/src/test/java/com/vaadin/flow/router/DefaultRouteResolverTest.java
@@ -15,16 +15,13 @@
  */
 package com.vaadin.flow.router;
 
-import java.util.ArrayList;
 import java.util.Collections;
-import java.util.HashMap;
 import java.util.LinkedHashMap;
 import java.util.Map;
 import java.util.Set;
 import java.util.stream.Collectors;
 import java.util.stream.Stream;
 
-import com.fasterxml.jackson.annotation.JsonProperty;
 import org.junit.Assert;
 import org.junit.Rule;
 import org.junit.Test;
@@ -41,7 +38,6 @@
 import com.vaadin.flow.server.RouteRegistry;
 import com.vaadin.flow.internal.menu.MenuRegistry;
 import com.vaadin.flow.server.menu.AvailableViewInfo;
-import com.vaadin.flow.server.menu.RouteParamType;
 
 public class DefaultRouteResolverTest extends RoutingTestBase {
 
@@ -149,6 +145,34 @@ public void clientRouteRequest_getDefinedLayout() {
         }
     }
 
+    @Test
+    public void clientRouteRequest_getDefinedLayoutAndParentLayouts() {
+        String path = "route";
+
+        router.getRegistry().setLayout(DefaultWithParentLayout.class);
+
+        try (MockedStatic<MenuRegistry> menuRegistry = Mockito
+                .mockStatic(MenuRegistry.class)) {
+            menuRegistry.when(() -> MenuRegistry.getClientRoutes(false))
+                    .thenReturn(Collections.singletonMap("/route",
+                            new AvailableViewInfo("", null, false, "/route",
+                                    false, false, null, null, null, true)));
+            NavigationState greeting = resolveNavigationState(path);
+            Assert.assertEquals(
+                    "Layout should be returned for a non server route when matching @Layout exists",
+                    DefaultWithParentLayout.class,
+                    greeting.getRouteTarget().getTarget());
+            Assert.assertEquals(
+                    "@ParentLayout annotation should be followed. @Layout class should not be in parent layout list.",
+                    1, greeting.getRouteTarget().getParentLayouts().size());
+            Assert.assertEquals(
+                    "@ParentLayout annotation should be followed. @Layout class should not be in parent layout list.",
+                    DefaultParentLayout.class,
+                    greeting.getRouteTarget().getParentLayouts().get(0));
+
+        }
+    }
+
     @Test
     public void clientRouteRequest_withRouteParameters_getDefinedLayout() {
         router.getRegistry().setLayout(DefaultLayout.class);
@@ -308,6 +332,18 @@ private static class DefaultLayout extends Component
             implements RouterLayout {
     }
 
+    @Tag("div")
+    @Layout
+    @ParentLayout(DefaultParentLayout.class)
+    private static class DefaultWithParentLayout extends Component
+            implements RouterLayout {
+    }
+
+    @Tag("div")
+    private static class DefaultParentLayout extends Component
+            implements RouterLayout {
+    }
+
     private Class<? extends Component> resolveNavigationTarget(String path) {
         return resolveNavigationState(path).getNavigationTarget();
     }