diff --git a/src/js/node/_http_server.ts b/src/js/node/_http_server.ts
index 5327cb01cc..e7f60c5450 100644
--- a/src/js/node/_http_server.ts
+++ b/src/js/node/_http_server.ts
@@ -611,6 +611,8 @@ Server.prototype[kRealListen] = function (tls, port, host, socketPath, reusePort
           http_res.end();
           socket.destroy();
         } else if (is_upgrade) {
+          // Enable streaming for WebSocket/upgrade connections
+          socket[kEnableStreaming](true);
           server.emit("upgrade", http_req, socket, kEmptyBuffer);
           if (!socket._httpMessage) {
             if (canUseInternalAssignSocket) {
diff --git a/test/js/node/http/http-websocket-upgrade.test.ts b/test/js/node/http/http-websocket-upgrade.test.ts
new file mode 100644
index 0000000000..289d185035
--- /dev/null
+++ b/test/js/node/http/http-websocket-upgrade.test.ts
@@ -0,0 +1,108 @@
+import { expect, test } from "bun:test";
+import { createHash } from "node:crypto";
+import { createServer } from "node:http";
+import { Socket } from "node:net";
+
+test("http.Server WebSocket upgrade sends response correctly", async () => {
+  const server = createServer((req, res) => {
+    res.writeHead(200);
+    res.end("OK");
+  });
+
+  let upgradeReceived = false;
+  let clientReceivedUpgrade = false;
+
+  server.on("upgrade", (request, socket, head) => {
+    upgradeReceived = true;
+
+    const key = request.headers["sec-websocket-key"];
+    expect(key).toBeTruthy();
+
+    if (!key) {
+      socket.destroy();
+      return;
+    }
+
+    // Generate WebSocket accept key
+    const acceptKey = createHash("sha1")
+      .update(key + "258EAFA5-E914-47DA-95CA-C5AB0DC85B11")
+      .digest("base64");
+
+    // Send WebSocket upgrade response
+    const headers = [
+      "HTTP/1.1 101 Switching Protocols",
+      "Upgrade: websocket",
+      "Connection: Upgrade",
+      `Sec-WebSocket-Accept: ${acceptKey}`,
+      "",
+      "",
+    ].join("\r\n");
+
+    socket.write(headers);
+  });
+
+  await new Promise<void>(resolve => {
+    server.listen(0, () => {
+      resolve();
+    });
+  });
+
+  const address = server.address();
+  if (!address || typeof address === "string") {
+    throw new Error("Server address is not valid");
+  }
+
+  // Create WebSocket client
+  const client = new Socket();
+
+  await new Promise<void>((resolve, reject) => {
+    const timeout = setTimeout(() => {
+      reject(new Error("Test timeout - client never received upgrade response"));
+    }, 2000);
+
+    client.connect(address.port, "127.0.0.1", () => {
+      // Send WebSocket handshake
+      const key = Buffer.from("testkey123456789").toString("base64");
+      const handshake = [
+        "GET /test HTTP/1.1",
+        "Host: localhost",
+        "Upgrade: websocket",
+        "Connection: Upgrade",
+        `Sec-WebSocket-Key: ${key}`,
+        "Sec-WebSocket-Version: 13",
+        "",
+        "",
+      ].join("\r\n");
+
+      client.write(handshake);
+    });
+
+    client.on("data", data => {
+      const response = data.toString();
+
+      if (response.includes("101 Switching Protocols")) {
+        clientReceivedUpgrade = true;
+        clearTimeout(timeout);
+        client.end();
+        resolve();
+      }
+    });
+
+    client.on("error", err => {
+      clearTimeout(timeout);
+      reject(err);
+    });
+  });
+
+  // Verify both server and client processed the upgrade
+  expect(upgradeReceived).toBe(true);
+  expect(clientReceivedUpgrade).toBe(true);
+
+  // Clean up
+  await new Promise<void>((resolve, reject) => {
+    server.close(err => {
+      if (err) reject(err);
+      else resolve();
+    });
+  });
+});