diff --git a/src/js/node/_http_server.ts b/src/js/node/_http_server.ts
index 282248b5675b..ccf3e3d214b2 100644
--- a/src/js/node/_http_server.ts
+++ b/src/js/node/_http_server.ts
@@ -1,7 +1,7 @@
 // Hardcoded module "node:_http_server"
 const EventEmitter: typeof import("node:events").EventEmitter = require("node:events");
 const { Stream } = require("node:stream");
-const { Socket: NetSocket } = require("node:net");
+const { Socket: NetSocket, Server: NetServer } = require("node:net");
 const {
   _checkInvalidHeaderChar: checkInvalidHeaderChar,
   chunkExpression,
@@ -276,7 +276,7 @@ function emitRequestCloseNT(self) {
 }
 
 function emitListeningNextTick(self, hostname, port) {
-  if ((self.listening = !!self[serverSymbol])) {
+  if (self[serverSymbol]) {
     // TODO: remove the arguments
     // Note does not pass any arguments.
     self.emit("listening", null, hostname, port);
@@ -301,7 +301,6 @@ function Server(options, callback): void {
   EventEmitter.$call(this);
   this.on("listening", setupConnectionsTracking);
 
-  this.listening = false;
   this._unref = false;
   this.timeout = 0;
   this.maxRequestsPerSocket = 0;
@@ -406,7 +405,18 @@ function Server(options, callback): void {
   if (callback) this.on("request", callback);
   return this;
 }
-$toClass(Server, "Server", EventEmitter);
+$toClass(Server, "Server", NetServer);
+
+// http.Server is backed by Bun.serve (held in [serverSymbol]); net.Server's
+// `listening` getter keys off `_handle`, which http.Server never populates.
+Object.defineProperty(Server.prototype, "listening", {
+  __proto__: null,
+  get() {
+    return !!this[serverSymbol];
+  },
+  configurable: true,
+  enumerable: true,
+});
 
 Server.prototype[kIncomingMessage] = undefined;
 
@@ -478,7 +488,6 @@ Server.prototype.closeAllConnections = function () {
   }
   this[serverSymbol] = undefined;
   clearInterval(this[kConnectionsCheckingInterval]);
-  this.listening = false;
 
   server.stop(true);
 };
@@ -510,7 +519,6 @@ Server.prototype.close = function (optionalCallback?) {
   }
   this[serverSymbol] = undefined;
   if (typeof optionalCallback === "function") setCloseCallback(this, optionalCallback);
-  this.listening = false;
   server.closeIdleConnections();
   server.stop();
   return this;
diff --git a/test/js/node/http/node-http.test.ts b/test/js/node/http/node-http.test.ts
index a204e6d37259..1cc82940fbd5 100644
--- a/test/js/node/http/node-http.test.ts
+++ b/test/js/node/http/node-http.test.ts
@@ -24,7 +24,7 @@ import http, {
 } from "node:http";
 import https, { createServer as createHttpsServer } from "node:https";
 import type { AddressInfo } from "node:net";
-import { connect, createServer as createNetServer } from "node:net";
+import net, { connect, createServer as createNetServer } from "node:net";
 import { tmpdir } from "node:os";
 import * as path from "node:path";
 import { PassThrough, Writable } from "node:stream";
@@ -145,6 +145,29 @@ describe("node:http", () => {
       listenResponse.close();
     });
 
+    // https://github.com/oven-sh/bun/issues/4360
+    it("http.Server inherits from net.Server", async () => {
+      expect(http.Server.prototype instanceof net.Server).toBe(true);
+      expect(net.Server.prototype instanceof http.Server).toBe(false);
+      expect(Object.getPrototypeOf(http.Server.prototype)).toBe(net.Server.prototype);
+      expect(Object.getPrototypeOf(http.Server)).toBe(net.Server);
+
+      const server = createServer();
+      expect(server instanceof http.Server).toBe(true);
+      expect(server instanceof net.Server).toBe(true);
+      expect(server instanceof EventEmitter).toBe(true);
+
+      expect(server.listening).toBe(false);
+      server.listen(0);
+      try {
+        await once(server, "listening");
+        expect(server.listening).toBe(true);
+      } finally {
+        server.close();
+      }
+      expect(server.listening).toBe(false);
+    });
+
     it("listen callback should be bound to server", async () => {
       const server = createServer();
       const { resolve, reject, promise } = Promise.withResolvers();