diff --git a/connectors/netty-connector/src/main/java/org/glassfish/jersey/netty/connector/NettyConnector.java b/connectors/netty-connector/src/main/java/org/glassfish/jersey/netty/connector/NettyConnector.java
index 671e72a94f..e4d3e8d1fa 100644
--- a/connectors/netty-connector/src/main/java/org/glassfish/jersey/netty/connector/NettyConnector.java
+++ b/connectors/netty-connector/src/main/java/org/glassfish/jersey/netty/connector/NettyConnector.java
@@ -1,5 +1,5 @@
 /*
- * Copyright (c) 2016, 2024 Oracle and/or its affiliates. All rights reserved.
+ * Copyright (c) 2016, 2025 Oracle and/or its affiliates. All rights reserved.
  *
  * This program and the accompanying materials are made available under the
  * terms of the Eclipse Public License v. 2.0, which is available at
@@ -17,7 +17,9 @@
 package org.glassfish.jersey.netty.connector;
 
 import java.io.IOException;
+import java.io.InterruptedIOException;
 import java.io.OutputStream;
+import java.io.OutputStreamWriter;
 import java.net.InetSocketAddress;
 import java.net.SocketAddress;
 import java.net.URI;
@@ -462,10 +464,15 @@ public void operationComplete(io.netty.util.concurrent.Future<? super Void> futu
                 jerseyRequest.setStreamProvider(new OutboundMessageContext.StreamProvider() {
                     @Override
                     public OutputStream getOutputStream(int contentLength) throws IOException {
-                        replaceHeaders(jerseyRequest, nettyRequest.headers()); // WriterInterceptor changes
-                        setHostHeader(jerseyRequest, nettyRequest);
-                        headersSet.countDown();
-
+                        try {
+                            replaceHeaders(jerseyRequest, nettyRequest.headers()); // WriterInterceptor changes
+                            setHostHeader(jerseyRequest, nettyRequest);
+                        } catch (Exception e) {
+                            responseDone.completeExceptionally(e);
+                            throw new IOException(e);
+                        } finally {
+                            headersSet.countDown();
+                        }
                         return entityWriter.getOutputStream();
                     }
                 });
diff --git a/connectors/netty-connector/src/test/java/org/glassfish/jersey/netty/connector/EmptyHeaderTest.java b/connectors/netty-connector/src/test/java/org/glassfish/jersey/netty/connector/EmptyHeaderTest.java
new file mode 100644
index 0000000000..fa1f5e8c69
--- /dev/null
+++ b/connectors/netty-connector/src/test/java/org/glassfish/jersey/netty/connector/EmptyHeaderTest.java
@@ -0,0 +1,82 @@
+/*
+ * Copyright (c) 2025 Oracle and/or its affiliates. All rights reserved.
+ *
+ * This program and the accompanying materials are made available under the
+ * terms of the Eclipse Public License v. 2.0, which is available at
+ * http://www.eclipse.org/legal/epl-2.0.
+ *
+ * This Source Code may also be made available under the following Secondary
+ * Licenses when the conditions for such availability set forth in the
+ * Eclipse Public License v. 2.0 are satisfied: GNU General Public License,
+ * version 2 with the GNU Classpath Exception, which is available at
+ * https://www.gnu.org/software/classpath/license.html.
+ *
+ * SPDX-License-Identifier: EPL-2.0 OR GPL-2.0 WITH Classpath-exception-2.0
+ */
+
+package org.glassfish.jersey.netty.connector;
+
+import org.glassfish.jersey.client.ClientConfig;
+import org.glassfish.jersey.server.ResourceConfig;
+import org.glassfish.jersey.test.JerseyTest;
+import org.junit.jupiter.api.Assertions;
+import org.junit.jupiter.api.Test;
+
+import javax.ws.rs.GET;
+import javax.ws.rs.Path;
+import javax.ws.rs.ProcessingException;
+import javax.ws.rs.client.ClientBuilder;
+import javax.ws.rs.client.Entity;
+import javax.ws.rs.core.Application;
+import javax.ws.rs.core.MediaType;
+import javax.ws.rs.core.MultivaluedHashMap;
+import javax.ws.rs.core.MultivaluedMap;
+import javax.ws.rs.core.Response;
+import java.util.Collections;
+import java.util.concurrent.ExecutionException;
+import java.util.logging.Logger;
+
+public class EmptyHeaderTest extends JerseyTest {
+
+    private static final Logger LOGGER = Logger.getLogger(EmptyHeaderTest.class.getName());
+
+    public static void main(String[] args) throws ExecutionException, InterruptedException {
+        new EmptyHeaderTest().testEmptyHeaders();
+    }
+
+    @Override
+    protected Application configure() {
+        return new ResourceConfig().register(new EmptyHeaderTestResource());
+    }
+
+    @Test
+    public void testEmptyHeaders() throws ExecutionException, InterruptedException {
+        MultivaluedMap<String, Object> jersey2Headers = new MultivaluedHashMap();
+        jersey2Headers.put("", Collections.singletonList("sss"));
+
+        Entity mData = Entity.entity("{\"dd\":\"ddd\"}", MediaType.APPLICATION_JSON_TYPE);
+
+        ClientConfig config = new ClientConfig();
+        config.connectorProvider(new NettyConnectorProvider());
+        try {
+            Response r = ClientBuilder.newBuilder()
+                    .withConfig(config)
+                    .build()
+                    .target(target().getUri())
+                    .request()
+                    .headers(jersey2Headers)
+                    .post(mData);
+            Assertions.fail("Processing Exception not thrown for empty header name");
+        } catch (ProcessingException processingException) {
+            System.out.println(processingException.getMessage());
+        }
+    }
+
+    @Path("")
+    private static class EmptyHeaderTestResource {
+        @GET
+        public Response ok() {
+            return Response.ok().build();
+        }
+    }
+}