diff --git a/src/js/node/_http_server.ts b/src/js/node/_http_server.ts
index 282248b5675b..623d85be3cbf 100644
--- a/src/js/node/_http_server.ts
+++ b/src/js/node/_http_server.ts
@@ -86,6 +86,7 @@ const OutgoingMessagePrototype = OutgoingMessage.prototype;
 const { kIncomingMessage } = require("node:_http_common");
 const kConnectionsCheckingInterval = Symbol("http.server.connectionsCheckingInterval");
 const kTrackedConnections = Symbol("http.server.trackedConnections");
+const kPendingDrainClose = Symbol("http.server.pendingDrainClose");
 const kHttpAllowHalfOpen = Symbol("http.server.httpAllowHalfOpen");
 
 // node.http trace events ('http.server.request' b/e). The agent module is
@@ -120,7 +121,14 @@ const DateNow = Date.now;
 let cluster;
 
 function emitCloseServer(self: Server) {
-  callCloseCallback(self);
+  // The native all-closed promise tracks pending requests, not open connections.
+  if (self[serverSymbol]) return;
+  const connections = self[kTrackedConnections];
+  if (connections && connections.size > 0) {
+    self[kPendingDrainClose] = true;
+    return;
+  }
+  self[kPendingDrainClose] = false;
   self.emit("close");
 }
 function emitCloseNTServer(this: Server) {
@@ -309,6 +317,7 @@ function Server(options, callback): void {
   defineHttpAllowHalfOpen(this);
   this[kInternalSocketData] = undefined;
   this[kTrackedConnections] = new Set();
+  this[kPendingDrainClose] = false;
   this[tlsSymbol] = null;
   this.noDelay = true;
   if (typeof options === "function") {
@@ -473,14 +482,18 @@ Server.prototype.unref = function () {
 
 Server.prototype.closeAllConnections = function () {
   const server = this[serverSymbol];
-  if (!server) {
+  if (server) {
+    this[serverSymbol] = undefined;
+    clearInterval(this[kConnectionsCheckingInterval]);
+    this.listening = false;
+    server.stop(true);
     return;
   }
-  this[serverSymbol] = undefined;
-  clearInterval(this[kConnectionsCheckingInterval]);
-  this.listening = false;
-
-  server.stop(true);
+  // close() already dropped the native handle; destroy what is still tracked.
+  const tracked = this[kTrackedConnections];
+  if (tracked && tracked.size > 0) {
+    for (const socket of Array.from(tracked)) socket.destroy();
+  }
 };
 
 Server.prototype.getConnections = function (callback) {
@@ -495,7 +508,16 @@ Server.prototype.getConnections = function (callback) {
 
 Server.prototype.closeIdleConnections = function () {
   const server = this[serverSymbol];
-  server?.closeIdleConnections();
+  if (server) {
+    server.closeIdleConnections();
+    return;
+  }
+  const tracked = this[kTrackedConnections];
+  if (tracked && tracked.size > 0) {
+    for (const socket of Array.from(tracked)) {
+      if (!socket._httpMessage) socket.destroy();
+    }
+  }
 };
 
 Server.prototype.close = function (optionalCallback?) {
@@ -509,7 +531,7 @@ Server.prototype.close = function (optionalCallback?) {
     return this;
   }
   this[serverSymbol] = undefined;
-  if (typeof optionalCallback === "function") setCloseCallback(this, optionalCallback);
+  if (typeof optionalCallback === "function") this.once("close", optionalCallback);
   this.listening = false;
   server.closeIdleConnections();
   server.stop();
@@ -1148,6 +1170,7 @@ Server.prototype[kRealListen] = function (tls, port, host, socketPath, reusePort
       // },
     });
 
+    this[kPendingDrainClose] = false;
     getBunServerAllClosedPromise(this[serverSymbol]).$then(emitCloseNTServer.bind(this));
     isHTTPS = this[serverSymbol].protocol === "https";
     applyServerCustomOptions(this);
@@ -1667,7 +1690,14 @@ const NodeHTTPServerSocket = class Socket extends NetSocket {
     // released parser (free() invoked, kOnTimeout nulled).
     releaseServerParserShim(this);
     this[kHandle] = null;
-    this.server?.[kTrackedConnections]?.delete(this);
+    const server = this.server;
+    const tracked = server?.[kTrackedConnections];
+    if (tracked) {
+      tracked.delete(this);
+      if (tracked.size === 0 && server[kPendingDrainClose]) {
+        process.nextTick(emitCloseServer, server);
+      }
+    }
     const timer = this[kSocketTimeoutTimer];
     if (timer) {
       clearTimeout(timer);
diff --git a/test/js/node/http/node-http-server-close-drain.test.ts b/test/js/node/http/node-http-server-close-drain.test.ts
new file mode 100644
index 000000000000..c23c9638c1c5
--- /dev/null
+++ b/test/js/node/http/node-http-server-close-drain.test.ts
@@ -0,0 +1,211 @@
+import { expect, test } from "bun:test";
+import { once } from "node:events";
+import { createServer } from "node:http";
+import type { AddressInfo } from "node:net";
+import { connect } from "node:net";
+
+// Node's net.Server#close callback (and the 'close' event) only fires once
+// every accepted connection has ended. A connection that was mid-request
+// when close() ran stays open after the response is delivered, so the
+// callback must be withheld until that connection closes.
+test("server.close(cb) does not fire while a keep-alive connection is still open", async () => {
+  const inHandler = Promise.withResolvers<void>();
+  let releaseResponse!: () => void;
+  const paths: string[] = [];
+  const server = createServer((req, res) => {
+    paths.push(req.url as string);
+    if (paths.length === 1) {
+      inHandler.resolve();
+      releaseResponse = () => res.end("resp:" + req.url);
+    } else {
+      res.end("resp:" + req.url);
+    }
+  });
+  server.keepAliveTimeout = 60000;
+  server.listen(0, "127.0.0.1");
+  await once(server, "listening");
+  const { port } = server.address() as AddressInfo;
+
+  const socket = connect(port, "127.0.0.1");
+  try {
+    await once(socket, "connect");
+    let body = "";
+    socket.on("data", chunk => (body += chunk));
+    socket.on("error", () => {});
+
+    // First request: handler is entered but response held until after close().
+    socket.write("GET /first HTTP/1.1\r\nHost: x\r\n\r\n");
+    await inHandler.promise;
+
+    let closeEventFired = false;
+    server.once("close", () => (closeEventFired = true));
+    const closed = Promise.withResolvers<void>();
+    let closeCbFired = false;
+    server.close(() => {
+      closeCbFired = true;
+      closed.resolve();
+    });
+
+    // Handler finishes: response is delivered, connection stays open.
+    // Yield a few event-loop turns after the bytes arrive so the server's
+    // "all requests done" task chain has run before the callback is checked.
+    releaseResponse();
+    while (!body.includes("resp:/first")) await once(socket, "data");
+    for (let i = 0; i < 4; i++) await new Promise<void>(r => setImmediate(r));
+    expect(closeCbFired).toBe(false);
+    expect(closeEventFired).toBe(false);
+
+    // A second request on the same connection is still served (matching Node),
+    // and the close callback must still be withheld afterwards.
+    socket.write("GET /second HTTP/1.1\r\nHost: x\r\n\r\n");
+    while (!body.includes("resp:/second")) await once(socket, "data");
+    for (let i = 0; i < 4; i++) await new Promise<void>(r => setImmediate(r));
+    expect(closeCbFired).toBe(false);
+    expect(closeEventFired).toBe(false);
+    expect(paths).toEqual(["/first", "/second"]);
+
+    // Closing the connection drains the server and releases the callback.
+    socket.destroy();
+    await closed.promise;
+    expect(closeCbFired).toBe(true);
+    expect(closeEventFired).toBe(true);
+  } finally {
+    socket.destroy();
+    server.closeAllConnections();
+  }
+});
+
+// Sanity: an idle keep-alive connection at close() time is reaped by
+// closeIdleConnections(), so the callback fires promptly like before.
+test("server.close(cb) fires once an idle keep-alive connection is reaped", async () => {
+  const server = createServer((req, res) => res.end("ok"));
+  server.keepAliveTimeout = 60000;
+  server.listen(0, "127.0.0.1");
+  await once(server, "listening");
+  const { port } = server.address() as AddressInfo;
+
+  const socket = connect(port, "127.0.0.1");
+  try {
+    await once(socket, "connect");
+    let body = "";
+    socket.on("data", chunk => (body += chunk));
+    socket.on("error", () => {});
+    socket.write("GET / HTTP/1.1\r\nHost: x\r\n\r\n");
+    while (!body.includes("ok")) await once(socket, "data");
+    for (let i = 0; i < 4; i++) await new Promise<void>(r => setImmediate(r));
+
+    const closed = Promise.withResolvers<void>();
+    server.close(() => closed.resolve());
+    await closed.promise;
+  } finally {
+    socket.destroy();
+    server.closeAllConnections();
+  }
+});
+
+// The graceful-drain-with-deadline pattern: close(), then force via
+// closeAllConnections() once the caller has waited long enough. The force
+// step must work even though close() already dropped the native handle.
+test("closeAllConnections() after close() force-drains the withheld callback", async () => {
+  const inHandler = Promise.withResolvers<void>();
+  let releaseResponse!: () => void;
+  const server = createServer((req, res) => {
+    inHandler.resolve();
+    releaseResponse = () => res.end("ok");
+  });
+  server.keepAliveTimeout = 60000;
+  server.listen(0, "127.0.0.1");
+  await once(server, "listening");
+  const { port } = server.address() as AddressInfo;
+
+  const socket = connect(port, "127.0.0.1");
+  try {
+    await once(socket, "connect");
+    let body = "";
+    socket.on("data", chunk => (body += chunk));
+    socket.on("error", () => {});
+    socket.write("GET / HTTP/1.1\r\nHost: x\r\n\r\n");
+    await inHandler.promise;
+
+    const closed = Promise.withResolvers<void>();
+    let closeCbFired = false;
+    server.close(() => {
+      closeCbFired = true;
+      closed.resolve();
+    });
+    releaseResponse();
+    while (!body.includes("ok")) await once(socket, "data");
+    for (let i = 0; i < 4; i++) await new Promise<void>(r => setImmediate(r));
+    expect(closeCbFired).toBe(false);
+
+    server.closeAllConnections();
+    await closed.promise;
+    expect(closeCbFired).toBe(true);
+  } finally {
+    socket.destroy();
+    server.closeAllConnections();
+  }
+});
+
+// Re-listening after close() while a keep-alive connection from the previous
+// cycle is still open must not fire 'close' on the new (listening) server
+// when that old connection finally ends.
+test("no 'close' is emitted on a re-listened server when an earlier connection ends", async () => {
+  const inHandler = Promise.withResolvers<void>();
+  let releaseResponse!: () => void;
+  let requests = 0;
+  const server = createServer((req, res) => {
+    if (++requests === 1) {
+      inHandler.resolve();
+      releaseResponse = () => res.end("ok");
+    } else {
+      res.end("ok");
+    }
+  });
+  server.keepAliveTimeout = 60000;
+  server.listen(0, "127.0.0.1");
+  await once(server, "listening");
+  const port1 = (server.address() as AddressInfo).port;
+
+  const socket = connect(port1, "127.0.0.1");
+  try {
+    await once(socket, "connect");
+    let body = "";
+    socket.on("data", chunk => (body += chunk));
+    socket.on("error", () => {});
+    socket.write("GET / HTTP/1.1\r\nHost: x\r\n\r\n");
+    await inHandler.promise;
+
+    let cb1Fired = false;
+    server.close(() => (cb1Fired = true));
+    releaseResponse();
+    while (!body.includes("ok")) await once(socket, "data");
+    for (let i = 0; i < 4; i++) await new Promise<void>(r => setImmediate(r));
+
+    // Re-listen while the old connection is still open.
+    server.listen(0, "127.0.0.1");
+    await once(server, "listening");
+
+    let closeEmitted = 0;
+    server.on("close", () => closeEmitted++);
+
+    // Old connection ends. No 'close' must fire on the listening server.
+    socket.destroy();
+    for (let i = 0; i < 4; i++) await new Promise<void>(r => setImmediate(r));
+    expect(closeEmitted).toBe(0);
+    expect(cb1Fired).toBe(false);
+    expect(server.listening).toBe(true);
+
+    // Closing the new server then emits 'close' exactly once. The first
+    // cycle's callback was registered via once('close') and fires now too,
+    // like Node (and passing a second callback does not throw).
+    const closed = Promise.withResolvers<void>();
+    server.close(() => closed.resolve());
+    await closed.promise;
+    expect(closeEmitted).toBe(1);
+    expect(cb1Fired).toBe(true);
+  } finally {
+    socket.destroy();
+    server.closeAllConnections();
+  }
+});