diff --git a/flow-push/pom.xml b/flow-push/pom.xml
index 19e15ec2694..f1e42f4c706 100644
--- a/flow-push/pom.xml
+++ b/flow-push/pom.xml
@@ -12,7 +12,7 @@
   <description>${project.name}</description>
 
   <properties>
-    <pushDirectory>${project.build.outputDirectory}/META-INF/resources/VAADIN/static/push</pushDirectory>
+    <pushDirectory>${project.build.outputDirectory}/META-INF/VAADIN/webapp/VAADIN/static/push</pushDirectory>
     <vaadinPush.js>${pushDirectory}/vaadinPush.js</vaadinPush.js>
     <vaadinPush-min.js>${pushDirectory}/vaadinPush-min.js</vaadinPush-min.js>
   </properties>
diff --git a/flow-server/src/test/java/com/vaadin/flow/server/StaticFileServerTest.java b/flow-server/src/test/java/com/vaadin/flow/server/StaticFileServerTest.java
index 43ea9bb8bce..e12a8f68ebf 100644
--- a/flow-server/src/test/java/com/vaadin/flow/server/StaticFileServerTest.java
+++ b/flow-server/src/test/java/com/vaadin/flow/server/StaticFileServerTest.java
@@ -1252,6 +1252,51 @@ public void serveStaticResource_themeResourceRequest_productionMode_notServeFrom
         Assert.assertFalse(fileServer.serveStaticResource(request, response));
     }
 
+    @Test
+    public void serveStaticResource_vaadinPushScript_servedFromMetaInfVaadinWebapp()
+            throws IOException {
+        String pathInfo = "/VAADIN/static/push/vaadinPush.js";
+        setupRequestURI("", "", pathInfo);
+        String fileData = "window.vaadinPush = {};";
+        ClassLoader mockLoader = Mockito.mock(ClassLoader.class);
+        Mockito.when(servletService.getClassLoader()).thenReturn(mockLoader);
+
+        // The push script should be loaded from META-INF/VAADIN/webapp/
+        // (not from META-INF/resources/VAADIN/static/push/)
+        Mockito.when(mockLoader.getResource(
+                "META-INF/VAADIN/webapp/VAADIN/static/push/vaadinPush.js"))
+                .thenReturn(createFileURLWithDataAndLength(
+                        "/push/vaadinPush.js", fileData));
+
+        mockStatsBundles(mockLoader);
+        mockConfigurationPolyfills();
+
+        Assert.assertTrue(fileServer.serveStaticResource(request, response));
+        Assert.assertEquals(fileData, out.getOutputString());
+    }
+
+    @Test
+    public void serveStaticResource_vaadinPushMinScript_servedFromMetaInfVaadinWebapp()
+            throws IOException {
+        String pathInfo = "/VAADIN/static/push/vaadinPush-min.js";
+        setupRequestURI("", "", pathInfo);
+        String fileData = "window.vaadinPush={};";
+        ClassLoader mockLoader = Mockito.mock(ClassLoader.class);
+        Mockito.when(servletService.getClassLoader()).thenReturn(mockLoader);
+
+        // The push script should be loaded from META-INF/VAADIN/webapp/
+        Mockito.when(mockLoader.getResource(
+                "META-INF/VAADIN/webapp/VAADIN/static/push/vaadinPush-min.js"))
+                .thenReturn(createFileURLWithDataAndLength(
+                        "/push/vaadinPush-min.js", fileData));
+
+        mockStatsBundles(mockLoader);
+        mockConfigurationPolyfills();
+
+        Assert.assertTrue(fileServer.serveStaticResource(request, response));
+        Assert.assertEquals(fileData, out.getOutputString());
+    }
+
     private static class CapturingServletOutputStream
             extends ServletOutputStream {
         ByteArrayOutputStream baos = new ByteArrayOutputStream();