diff --git a/webserver/tests/websocket/src/test/java/io/helidon/webserver/tests/websocket/WebSocketSupplierTest.java b/webserver/tests/websocket/src/test/java/io/helidon/webserver/tests/websocket/WebSocketSupplierTest.java
new file mode 100644
index 00000000000..f9ee326cb01
--- /dev/null
+++ b/webserver/tests/websocket/src/test/java/io/helidon/webserver/tests/websocket/WebSocketSupplierTest.java
@@ -0,0 +1,81 @@
+/*
+ * Copyright (c) 2023 Oracle and/or its affiliates.
+ *
+ * Licensed under the Apache License, Version 2.0 (the "License");
+ * you may not use this file except in compliance with the License.
+ * You may obtain a copy of the License at
+ *
+ *     http://www.apache.org/licenses/LICENSE-2.0
+ *
+ * Unless required by applicable law or agreed to in writing, software
+ * distributed under the License is distributed on an "AS IS" BASIS,
+ * WITHOUT WARRANTIES OR CONDITIONS OF ANY KIND, either express or implied.
+ * See the License for the specific language governing permissions and
+ * limitations under the License.
+ */
+
+package io.helidon.webserver.tests.websocket;
+
+import java.net.URI;
+import java.net.http.HttpClient;
+import java.time.Duration;
+import java.util.concurrent.TimeUnit;
+import java.util.concurrent.atomic.AtomicInteger;
+import java.util.function.Supplier;
+
+import io.helidon.webserver.Router;
+import io.helidon.webserver.WebServer;
+import io.helidon.webserver.testing.junit5.ServerTest;
+import io.helidon.webserver.testing.junit5.SetUpRoute;
+import io.helidon.webserver.websocket.WsRouting;
+import io.helidon.websocket.WsCloseCodes;
+import io.helidon.websocket.WsListener;
+import org.junit.jupiter.api.Test;
+
+import static org.hamcrest.CoreMatchers.is;
+import static org.hamcrest.MatcherAssert.assertThat;
+
+/**
+ * Checks that a {@code WsListener} supplier is called exactly once per connection.
+ * In particular, that the same listener is shared between the connection upgrade
+ * and the connection handling phases.
+ */
+@ServerTest
+class WebSocketSupplierTest {
+
+    private final int port;
+    private final HttpClient client;
+
+    private static final AtomicInteger supplierCalls = new AtomicInteger();
+
+    WebSocketSupplierTest(WebServer server) {
+        port = server.port();
+        client = HttpClient.newBuilder()
+                .connectTimeout(Duration.ofSeconds(5))
+                .build();
+    }
+
+    @SetUpRoute
+    static void router(Router.RouterBuilder<?> router) {
+        Supplier<WsListener> supplier = () -> {
+            EchoService service = new EchoService();
+            supplierCalls.getAndIncrement();
+            return service;
+        };
+        router.addRouting(WsRouting.builder().endpoint("/echo", supplier));
+    }
+
+    @Test
+    void testSingleSupplier() throws Exception {
+        java.net.http.WebSocket ws = client.newWebSocketBuilder()
+                .buildAsync(URI.create("ws://localhost:" + port + "/echo"),
+                        new java.net.http.WebSocket.Listener() {})
+                .get(5, TimeUnit.SECONDS);
+        ws.request(10);
+        ws.sendText("Hello", true).get(5, TimeUnit.SECONDS);
+        ws.sendClose(WsCloseCodes.NORMAL_CLOSE, "normal").get(5, TimeUnit.SECONDS);
+
+        // enforce one listener per connection -- single call to supplier
+        assertThat(supplierCalls.get(), is(1));
+    }
+}
diff --git a/webserver/websocket/src/main/java/io/helidon/webserver/websocket/WsConnection.java b/webserver/websocket/src/main/java/io/helidon/webserver/websocket/WsConnection.java
index 32d3f442d88..198d2ac4d0a 100644
--- a/webserver/websocket/src/main/java/io/helidon/webserver/websocket/WsConnection.java
+++ b/webserver/websocket/src/main/java/io/helidon/webserver/websocket/WsConnection.java
@@ -70,12 +70,12 @@ private WsConnection(ConnectionContext ctx,
                          HttpPrologue prologue,
                          Headers upgradeHeaders,
                          String wsKey,
-                         WsRoute wsRoute) {
+                         WsListener wsListener) {
         this.ctx = ctx;
         this.prologue = prologue;
         this.upgradeHeaders = upgradeHeaders;
         this.wsKey = wsKey;
-        this.listener = wsRoute.listener();
+        this.listener = wsListener;
         this.dataReader = ctx.dataReader();
         this.lastRequestTimestamp = DateTime.timestamp();
         this.wsConfig = (WsConfig) ctx.listenerContext()
@@ -94,15 +94,15 @@ private WsConnection(ConnectionContext ctx,
      * @param prologue       prologue of this request
      * @param upgradeHeaders headers for
      * @param wsKey          ws key
-     * @param wsRoute        route to use
+     * @param wsListener     a ws listener
      * @return a new connection
      */
     public static WsConnection create(ConnectionContext ctx,
                                       HttpPrologue prologue,
                                       Headers upgradeHeaders,
                                       String wsKey,
-                                      WsRoute wsRoute) {
-        return new WsConnection(ctx, prologue, upgradeHeaders, wsKey, wsRoute);
+                                      WsListener wsListener) {
+        return new WsConnection(ctx, prologue, upgradeHeaders, wsKey, wsListener);
     }
 
     @Override
diff --git a/webserver/websocket/src/main/java/io/helidon/webserver/websocket/WsUpgrader.java b/webserver/websocket/src/main/java/io/helidon/webserver/websocket/WsUpgrader.java
index 476e351ecfc..71f21ca49a0 100644
--- a/webserver/websocket/src/main/java/io/helidon/webserver/websocket/WsUpgrader.java
+++ b/webserver/websocket/src/main/java/io/helidon/webserver/websocket/WsUpgrader.java
@@ -38,6 +38,7 @@
 import io.helidon.webserver.ConnectionContext;
 import io.helidon.webserver.http1.spi.Http1Upgrader;
 import io.helidon.webserver.spi.ServerConnection;
+import io.helidon.websocket.WsListener;
 import io.helidon.websocket.WsUpgradeException;
 
 import static java.nio.charset.StandardCharsets.US_ASCII;
@@ -167,8 +168,9 @@ public ServerConnection upgrade(ConnectionContext ctx, HttpPrologue prologue, Wr
 
         // invoke user-provided HTTP upgrade handler
         Optional<Headers> upgradeHeaders;
+        WsListener wsListener = route.listener();
         try {
-            upgradeHeaders = route.listener().onHttpUpgrade(prologue, headers);
+            upgradeHeaders = wsListener.onHttpUpgrade(prologue, headers);
         } catch (WsUpgradeException e) {
             LOGGER.log(Level.TRACE, "Websocket upgrade rejected", e);
             return null;
@@ -191,7 +193,7 @@ public ServerConnection upgrade(ConnectionContext ctx, HttpPrologue prologue, Wr
             LOGGER.log(Level.TRACE, "Upgraded to websocket version " + version);
         }
 
-        return WsConnection.create(ctx, prologue, upgradeHeaders.orElse(EMPTY_HEADERS), wsKey, route);
+        return WsConnection.create(ctx, prologue, upgradeHeaders.orElse(EMPTY_HEADERS), wsKey, wsListener);
     }
 
     protected boolean anyOrigin() {