diff --git a/lib/websocket-server.js b/lib/websocket-server.js
index 4fc5bad24..7e992c2a2 100644
--- a/lib/websocket-server.js
+++ b/lib/websocket-server.js
@@ -10,6 +10,7 @@ const { format, parse } = require('./extension');
 const { GUID } = require('./constants');
 
 const keyRegex = /^[+/0-9A-Za-z]{22}==$/;
+const kUsedByWebSocketServer = Symbol('kUsedByWebSocketServer');
 
 /**
  * Class representing a WebSocket server.
@@ -82,6 +83,14 @@ class WebSocketServer extends EventEmitter {
     }
 
     if (this._server) {
+      if (this._server[kUsedByWebSocketServer]) {
+        throw new Error(
+          'The HTTP/S server is already being used by another WebSocket server'
+        );
+      } else {
+        this._server[kUsedByWebSocketServer] = true;
+      }
+
       this._removeListeners = addListeners(this._server, {
         listening: this.emit.bind(this, 'listening'),
         error: this.emit.bind(this, 'error'),
@@ -135,6 +144,8 @@ class WebSocketServer extends EventEmitter {
     const server = this._server;
 
     if (server) {
+      server[kUsedByWebSocketServer] = false;
+
       this._removeListeners();
       this._removeListeners = this._server = null;
 
diff --git a/test/websocket-server.test.js b/test/websocket-server.test.js
index 5d152ab73..b9c460ce4 100644
--- a/test/websocket-server.test.js
+++ b/test/websocket-server.test.js
@@ -17,11 +17,22 @@ describe('WebSocketServer', () => {
       assert.throws(() => new WebSocket.Server());
     });
 
-    it('throws an error if no port or server is specified', () => {
-      assert.throws(() => new WebSocket.Server({}));
-    });
-
     describe('options', () => {
+      it('throws an error if no `port` or `server` option is specified', () => {
+        assert.throws(() => new WebSocket.Server({}));
+      });
+
+      it('throws an error if the server is already being used', () => {
+        const server = http.createServer();
+
+        new WebSocket.Server({ server });
+
+        assert.throws(
+          () => new WebSocket.Server({ server }),
+          /^Error: The HTTP\/S server is already being used by another WebSocket server$/
+        );
+      });
+
       it('exposes options passed to constructor', (done) => {
         const wss = new WebSocket.Server({ port: 0 }, () => {
           assert.strictEqual(wss.options.port, 0);
@@ -225,15 +236,21 @@ describe('WebSocketServer', () => {
 
     it('cleans event handlers on precreated server', (done) => {
       const server = http.createServer();
-      const wss = new WebSocket.Server({ server });
+      const wss1 = new WebSocket.Server({ server });
 
       server.listen(0, () => {
-        wss.close(() => {
+        wss1.close(() => {
           assert.strictEqual(server.listenerCount('listening'), 0);
           assert.strictEqual(server.listenerCount('upgrade'), 0);
           assert.strictEqual(server.listenerCount('error'), 0);
 
-          server.close(done);
+          // Check that no error is thrown if `server` is resued now as there
+          // are no other `WebSocketServer`s using it.
+          const wss2 = new WebSocket.Server({ server });
+
+          wss2.close(() => {
+            server.close(done);
+          });
         });
       });
     });