diff --git a/vertx-core/src/main/java/io/vertx/core/net/impl/VertxConnection.java b/vertx-core/src/main/java/io/vertx/core/net/impl/VertxConnection.java
index 5d93897e3cb..6ed702c6ea7 100644
--- a/vertx-core/src/main/java/io/vertx/core/net/impl/VertxConnection.java
+++ b/vertx-core/src/main/java/io/vertx/core/net/impl/VertxConnection.java
@@ -463,8 +463,8 @@ public final void doResume() {
       return;
     }
     paused = false;
-    if (pending != null) {
-      assert !read;
+    if (pending != null && !pending.isEmpty()) {
+      boolean end = !read;
       read = true;
       try {
         Object msg;
@@ -472,7 +472,9 @@ public final void doResume() {
           handleMessage(msg);
         }
       } finally {
-        endReadAndFlush();
+        if (end) {
+          endReadAndFlush();
+        }
         if (pending.isEmpty() && !autoRead) {
           autoRead = true;
           chctx.channel().config().setAutoRead(true);
diff --git a/vertx-core/src/test/java/io/vertx/tests/deployment/VirtualThreadDeploymentTest.java b/vertx-core/src/test/java/io/vertx/tests/deployment/VirtualThreadDeploymentTest.java
index 525e02d4016..5ea96989b42 100644
--- a/vertx-core/src/test/java/io/vertx/tests/deployment/VirtualThreadDeploymentTest.java
+++ b/vertx-core/src/test/java/io/vertx/tests/deployment/VirtualThreadDeploymentTest.java
@@ -192,9 +192,7 @@ public Future<?> start() throws Exception {
                   .compose(HttpClientRequest::send)
                   .await();
               } catch (Throwable e) {
-                if (e instanceof InterruptedException) {
-                  interruptedThreads.add(Thread.currentThread());
-                }
+                interruptedThreads.add(Thread.currentThread());
               }
             });
           }
diff --git a/vertx-core/src/test/java/io/vertx/tests/net/ConnectionBaseTest.java b/vertx-core/src/test/java/io/vertx/tests/net/ConnectionBaseTest.java
index 14dec4106f6..91e7daad049 100644
--- a/vertx-core/src/test/java/io/vertx/tests/net/ConnectionBaseTest.java
+++ b/vertx-core/src/test/java/io/vertx/tests/net/ConnectionBaseTest.java
@@ -634,4 +634,30 @@ public void testPauseWhenResuming() {
     ch.runPendingTasks();
     assertEquals(2, count.get());
   }
+
+  @Test
+  public void testResumeWhenReadInProgress() {
+    MessageFactory factory = new MessageFactory();
+    EmbeddedChannel ch = new EmbeddedChannel();
+    ChannelPipeline pipeline = ch.pipeline();
+    pipeline.addLast(VertxHandler.create(chctx -> new TestConnection(chctx)));
+    TestConnection connection = (TestConnection) pipeline.get(VertxHandler.class).getConnection();
+    AtomicInteger count = new AtomicInteger();
+    connection.handler = event -> count.incrementAndGet();
+    connection.pause();
+    pipeline.fireChannelRead(factory.next());
+    assertEquals(0, count.get());
+    Object expected = new Object();
+    connection.write(expected, false, ch.newPromise());
+    connection.resume();
+    assertEquals(0, count.get());
+    assertTrue(ch.hasPendingTasks());
+    ch.runPendingTasks();
+    assertEquals(1, count.get());
+    Object outbound = ch.readOutbound();
+    assertNull(outbound);
+    pipeline.fireChannelReadComplete();
+    outbound = ch.readOutbound();
+    assertSame(expected, outbound);
+  }
 }