diff --git a/flow-server/src/main/java/com/vaadin/flow/server/startup/DevModeInitializer.java b/flow-server/src/main/java/com/vaadin/flow/server/startup/DevModeInitializer.java
index ee60e1f4b5b..e8d1d20665e 100644
--- a/flow-server/src/main/java/com/vaadin/flow/server/startup/DevModeInitializer.java
+++ b/flow-server/src/main/java/com/vaadin/flow/server/startup/DevModeInitializer.java
@@ -89,6 +89,7 @@
 import elemental.json.JsonObject;
 
 import static com.vaadin.flow.server.Constants.PACKAGE_JSON;
+import static com.vaadin.flow.server.Constants.VAADIN_SERVLET_RESOURCES;
 import static com.vaadin.flow.server.InitParameters.SERVLET_PARAMETER_DEVMODE_OPTIMIZE_BUNDLE;
 import static com.vaadin.flow.server.frontend.FrontendUtils.DEFAULT_FRONTEND_DIR;
 import static com.vaadin.flow.server.frontend.FrontendUtils.DEFAULT_GENERATED_DIR;
@@ -287,10 +288,11 @@ public static void initDevModeHandler(Set<Class<?>> classes,
 
         File generatedPackages = new File(builder.generatedFolder,
                 PACKAGE_JSON);
-
+        File target = new File(baseDir, "target");
         // Always update to auto-generated webpack configuration
-        builder.withWebpack(builder.npmFolder, FrontendUtils.WEBPACK_CONFIG,
-                FrontendUtils.WEBPACK_GENERATED);
+        builder.withWebpack(
+                new File(target, "classes/" + VAADIN_SERVLET_RESOURCES),
+                FrontendUtils.WEBPACK_CONFIG, FrontendUtils.WEBPACK_GENERATED);
 
         // If we are missing either the base or generated package json files
         // generate those
diff --git a/flow-server/src/test/java/com/vaadin/flow/server/startup/DevModeInitializerTest.java b/flow-server/src/test/java/com/vaadin/flow/server/startup/DevModeInitializerTest.java
index 41ff49579fa..62182c62d6a 100644
--- a/flow-server/src/test/java/com/vaadin/flow/server/startup/DevModeInitializerTest.java
+++ b/flow-server/src/test/java/com/vaadin/flow/server/startup/DevModeInitializerTest.java
@@ -23,6 +23,8 @@
 import java.util.List;
 import java.util.Set;
 import java.util.function.Function;
+import java.util.regex.Matcher;
+import java.util.regex.Pattern;
 
 import net.jcip.annotations.NotThreadSafe;
 
@@ -245,6 +247,33 @@ public void should_Always_Update_Generated_Webpack_Conf() throws Exception {
         }
     }
 
+    @Test
+    public void generated_output_should_be_in_target_classes()
+            throws Exception {
+        File generatedWebpackFile = new File(webpackFile.getParentFile(),
+                FrontendUtils.WEBPACK_GENERATED);
+        try (FileWriter writer = new FileWriter(generatedWebpackFile)) {
+            process();
+
+            final String generated = IOUtils.toString(
+                    generatedWebpackFile.toURI(), StandardCharsets.UTF_8);
+
+            final Pattern compile = Pattern.compile(
+                    "projectStaticAssetsOutputFolder.* '(.*)'");
+            final Matcher matcher = compile.matcher(generated);
+            matcher.find();
+
+            Assert.assertTrue(
+                    "Generated webpack configuration contained faulty path ´"
+                            + matcher.group(1)
+                            + "' instead of 'target/classes/META-INF/VAADIN/static'",
+                    generated.contains(
+                            "const projectStaticAssetsOutputFolder = require('path').resolve(__dirname, 'target/classes/META-INF/VAADIN/static');"));
+        } finally {
+            generatedWebpackFile.delete();
+        }
+    }
+
     @Test
     public void should_Run_Updaters_doesNotThrow() throws Exception {
         // no any exception means that updaters are executed and dev mode server