diff --git a/ext/http/00_serve.ts b/ext/http/00_serve.ts
index 7c665ac154d53b..84b8cd321b0672 100644
--- a/ext/http/00_serve.ts
+++ b/ext/http/00_serve.ts
@@ -753,26 +753,52 @@ function serveHttpOn(context, addr, callback) {
       PromisePrototypeCatch(callback(req), promiseErrorHandler);
     }
 
-    if (!context.closing && !context.closed) {
-      context.closing = op_http_close(rid, false);
+    try {
+      if (!context.closing && !context.closed) {
+        context.closing = await op_http_close(rid, false);
+        context.close();
+      }
+
+      await context.closing;
+    } catch (error) {
+      if (ObjectPrototypeIsPrototypeOf(InterruptedPrototype, error)) {
+        return;
+      }
+      if (ObjectPrototypeIsPrototypeOf(BadResourcePrototype, error)) {
+        return;
+      }
+
+      throw error;
+    } finally {
       context.close();
+      context.closed = true;
     }
-
-    await context.closing;
-    context.close();
-    context.closed = true;
   })();
 
   return {
     addr,
     finished,
     async shutdown() {
-      if (!context.closing && !context.closed) {
-        // Shut this HTTP server down gracefully
-        context.closing = op_http_close(context.serverRid, true);
+      try {
+        if (!context.closing && !context.closed) {
+          // Shut this HTTP server down gracefully
+          context.closing = op_http_close(context.serverRid, true);
+        }
+
+        await context.closing;
+      } catch (error) {
+        // The server was interrupted
+        if (ObjectPrototypeIsPrototypeOf(InterruptedPrototype, error)) {
+          return;
+        }
+        if (ObjectPrototypeIsPrototypeOf(BadResourcePrototype, error)) {
+          return;
+        }
+
+        throw error;
+      } finally {
+        context.closed = true;
       }
-      await context.closing;
-      context.closed = true;
     },
     ref() {
       ref = true;
diff --git a/ext/node/polyfills/http.ts b/ext/node/polyfills/http.ts
index 32e69772d6cdd7..c6c112a508a744 100644
--- a/ext/node/polyfills/http.ts
+++ b/ext/node/polyfills/http.ts
@@ -1775,8 +1775,12 @@ export class ServerImpl extends EventEmitter {
     }
 
     if (listening && this.#ac) {
-      this.#ac.abort();
-      this.#ac = undefined;
+      if (this.#server) {
+        this.#server.shutdown();
+      } else if (this.#ac) {
+        this.#ac.abort();
+        this.#ac = undefined;
+      }
     } else {
       this.#serveDeferred!.resolve();
     }
@@ -1785,6 +1789,26 @@ export class ServerImpl extends EventEmitter {
     return this;
   }
 
+  closeAllConnections() {
+    if (this.#hasClosed) {
+      return;
+    }
+    if (this.#ac) {
+      this.#ac.abort();
+      this.#ac = undefined;
+    }
+  }
+
+  closeIdleConnections() {
+    if (this.#hasClosed) {
+      return;
+    }
+
+    if (this.#server) {
+      this.#server.shutdown();
+    }
+  }
+
   address() {
     return {
       port: this.#addr.port,
diff --git a/tests/unit_node/http_test.ts b/tests/unit_node/http_test.ts
index 2b26442721e979..ca3c658adb84e4 100644
--- a/tests/unit_node/http_test.ts
+++ b/tests/unit_node/http_test.ts
@@ -2,6 +2,7 @@
 
 import EventEmitter from "node:events";
 import http, { type RequestOptions } from "node:http";
+import url from "node:url";
 import https from "node:https";
 import net from "node:net";
 import { assert, assertEquals, fail } from "@std/assert/mod.ts";
@@ -1040,3 +1041,66 @@ Deno.test("[node/http] ServerResponse default status code 200", () => {
 Deno.test("[node/http] maxHeaderSize is defined", () => {
   assertEquals(http.maxHeaderSize, 16_384);
 });
+
+Deno.test("[node/http] server graceful close", async () => {
+  const server = http.createServer(function (_, response) {
+    response.writeHead(200, {});
+    response.end("ok");
+    server.close();
+  });
+
+  const { promise, resolve } = Promise.withResolvers<void>();
+  server.listen(0, function () {
+    // deno-lint-ignore no-explicit-any
+    const port = (server.address() as any).port;
+    const testURL = url.parse(
+      `http://localhost:${port}`,
+    );
+
+    http.request(testURL, function (response) {
+      assertEquals(response.statusCode, 200);
+      response.on("data", function () {});
+      response.on("end", function () {
+        resolve();
+      });
+    }).end();
+  });
+
+  await promise;
+});
+
+Deno.test("[node/http] server closeAllConnections shutdown", async () => {
+  const server = http.createServer((_req, res) => {
+    res.writeHead(200, { "Content-Type": "application/json" });
+    res.end(JSON.stringify({
+      data: "Hello World!",
+    }));
+  });
+
+  server.listen(0);
+  const { promise, resolve } = Promise.withResolvers<void>();
+  setTimeout(() => {
+    server.close(() => resolve());
+    server.closeAllConnections();
+  }, 2000);
+
+  await promise;
+});
+
+Deno.test("[node/http] server closeIdleConnections shutdown", async () => {
+  const server = http.createServer({ keepAliveTimeout: 60000 }, (_req, res) => {
+    res.writeHead(200, { "Content-Type": "application/json" });
+    res.end(JSON.stringify({
+      data: "Hello World!",
+    }));
+  });
+
+  server.listen(0);
+  const { promise, resolve } = Promise.withResolvers<void>();
+  setTimeout(() => {
+    server.close(() => resolve());
+    server.closeIdleConnections();
+  }, 2000);
+
+  await promise;
+});