diff --git a/flow-server/src/main/java/com/vaadin/flow/server/communication/IndexHtmlRequestHandler.java b/flow-server/src/main/java/com/vaadin/flow/server/communication/IndexHtmlRequestHandler.java
index e7a901df2bd..b34dd19fbe2 100644
--- a/flow-server/src/main/java/com/vaadin/flow/server/communication/IndexHtmlRequestHandler.java
+++ b/flow-server/src/main/java/com/vaadin/flow/server/communication/IndexHtmlRequestHandler.java
@@ -39,6 +39,8 @@
 import elemental.json.JsonObject;
 import elemental.json.impl.JsonUtil;
 
+import java.io.File;
+
 import static com.vaadin.flow.component.internal.JavaScriptBootstrapUI.SERVER_ROUTING;
 import static com.vaadin.flow.shared.ApplicationConstants.CONTENT_TYPE_TEXT_HTML_UTF_8;
 import static com.vaadin.flow.shared.ApplicationConstants.CSRF_TOKEN;
@@ -172,10 +174,16 @@ private static Document getIndexHtmlDocument(VaadinRequest request)
         }
         String frontendDir = FrontendUtils.getProjectFrontendDir(
                 request.getService().getDeploymentConfiguration());
+        String indexHtmlFilePath;
+        if(frontendDir.endsWith(File.separator)) {
+            indexHtmlFilePath = frontendDir + "index.html";
+        } else {
+            indexHtmlFilePath = frontendDir + File.separatorChar + "index.html";
+        }
         String message = String
-                .format("Failed to load content of '%1$sindex.html'."
-                        + "It is required to have '%1$sindex.html' file when "
-                        + "using client side bootstrapping.", frontendDir);
+                .format("Failed to load content of '%1$s'. "
+                        + "It is required to have '%1$s' file when "
+                        + "using client side bootstrapping.", indexHtmlFilePath);
         throw new IOException(message);
     }
 
diff --git a/flow-server/src/test/java/com/vaadin/flow/server/communication/IndexHtmlRequestHandlerTest.java b/flow-server/src/test/java/com/vaadin/flow/server/communication/IndexHtmlRequestHandlerTest.java
index 11caa930571..9a455f1dfe6 100644
--- a/flow-server/src/test/java/com/vaadin/flow/server/communication/IndexHtmlRequestHandlerTest.java
+++ b/flow-server/src/test/java/com/vaadin/flow/server/communication/IndexHtmlRequestHandlerTest.java
@@ -21,6 +21,7 @@
 import java.io.File;
 import java.io.IOException;
 import java.lang.reflect.Method;
+import java.net.URL;
 import java.nio.charset.StandardCharsets;
 import java.util.Optional;
 import java.util.concurrent.CompletableFuture;
@@ -36,6 +37,7 @@
 import org.junit.Before;
 import org.junit.Rule;
 import org.junit.Test;
+import org.junit.rules.ExpectedException;
 import org.junit.rules.TemporaryFolder;
 import org.mockito.Mockito;
 
@@ -46,6 +48,7 @@
 import com.vaadin.flow.server.DevModeHandler;
 import com.vaadin.flow.server.MockServletServiceSessionSetup;
 import com.vaadin.flow.server.VaadinResponse;
+import com.vaadin.flow.server.VaadinService;
 import com.vaadin.flow.server.VaadinServletRequest;
 import com.vaadin.flow.server.VaadinSession;
 import com.vaadin.flow.server.frontend.FrontendUtils;
@@ -57,9 +60,13 @@
 import elemental.json.JsonObject;
 
 import static com.vaadin.flow.component.internal.JavaScriptBootstrapUI.SERVER_ROUTING;
+import static com.vaadin.flow.server.Constants.VAADIN_SERVLET_RESOURCES;
 import static com.vaadin.flow.server.DevModeHandlerTest.createStubWebpackTcpListener;
+import static com.vaadin.flow.server.frontend.FrontendUtils.INDEX_HTML;
 import static com.vaadin.flow.server.frontend.NodeUpdateTestUtil.createStubWebpackServer;
 import static org.junit.Assert.assertEquals;
+import static org.junit.Assert.assertNotNull;
+import static org.junit.Assert.assertTrue;
 
 public class IndexHtmlRequestHandlerTest {
     private MockServletServiceSessionSetup mocks;
@@ -73,6 +80,8 @@ public class IndexHtmlRequestHandlerTest {
 
     @Rule
     public final TemporaryFolder temporaryFolder = new TemporaryFolder();
+    @Rule
+    public ExpectedException exceptionRule = ExpectedException.none();
 
     @Before
     public void setUp() throws Exception {
@@ -103,6 +112,41 @@ public void serveIndexHtml_requestWithRootPath_serveContentFromTemplate()
                 indexHtml.contains(".v-system-error"));
     }
 
+    @Test
+    public void serveNotFoundIndexHtml_requestWithRootPath_failsWithIOException()
+            throws IOException {
+        VaadinServletRequest vaadinServletRequest = createVaadinRequest("/");
+        VaadinService vaadinService = vaadinServletRequest.getService();
+
+        // Finding index.html URL
+        String indexHtmlPathInProductionMode = VAADIN_SERVLET_RESOURCES
+                + INDEX_HTML;
+        URL url = vaadinService.getClassLoader().getResource(indexHtmlPathInProductionMode);
+
+        assertNotNull(url);
+        File indexHtmlFile = new File(url.getPath());
+        File indexHtmlFileTmp = new File(url.getPath() + "_tmp");
+        try {
+            // Renaming file to simulate the absence of index.html
+            boolean renamed = indexHtmlFile.renameTo(indexHtmlFileTmp);
+            assertTrue(renamed);
+
+            String expectedError = "Failed to load content of './frontend/index.html'. " +
+                    "It is required to have './frontend/index.html' file " +
+                    "when using client side bootstrapping.";
+
+            exceptionRule.expect(IOException.class);
+            exceptionRule.expectMessage(expectedError);
+
+            indexHtmlRequestHandler.synchronizedHandleRequest(session,
+                    vaadinServletRequest, response);
+        } finally {
+            // Restoring index.html
+            boolean renamed = indexHtmlFileTmp.renameTo(indexHtmlFile);
+            assertTrue(renamed);
+        }
+    }
+
     @Test
     public void serveIndexHtml_requestWithRootPath_hasBaseHrefElement()
             throws IOException {