diff --git a/codec-http2/src/main/java/io/netty/handler/codec/http2/DefaultHttp2LocalFlowController.java b/codec-http2/src/main/java/io/netty/handler/codec/http2/DefaultHttp2LocalFlowController.java
index 959f327a17..12116c8290 100644
--- a/codec-http2/src/main/java/io/netty/handler/codec/http2/DefaultHttp2LocalFlowController.java
+++ b/codec-http2/src/main/java/io/netty/handler/codec/http2/DefaultHttp2LocalFlowController.java
@@ -110,8 +110,11 @@ public class DefaultHttp2LocalFlowController implements Http2LocalFlowController
                     FlowState state = state(stream);
                     int unconsumedBytes = state.unconsumedBytes();
                     if (ctx != null && unconsumedBytes > 0) {
-                        connectionState().consumeBytes(unconsumedBytes);
-                        state.consumeBytes(unconsumedBytes);
+                        if (consumeAllBytes(state, unconsumedBytes)) {
+                            // As the user has no real control on when this callback is used we should better
+                            // call flush() if we produced any window update to ensure we not stale.
+                            ctx.flush();
+                        }
                     }
                 } catch (Http2Exception e) {
                     PlatformDependent.throwException(e);
@@ -187,13 +190,15 @@ public class DefaultHttp2LocalFlowController implements Http2LocalFlowController
                 throw new UnsupportedOperationException("Returning bytes for the connection window is not supported");
             }
 
-            boolean windowUpdateSent = connectionState().consumeBytes(numBytes);
-            windowUpdateSent |= state(stream).consumeBytes(numBytes);
-            return windowUpdateSent;
+            return consumeAllBytes(state(stream), numBytes);
         }
         return false;
     }
 
+    private boolean consumeAllBytes(FlowState state, int numBytes) throws Http2Exception {
+        return connectionState().consumeBytes(numBytes) | state.consumeBytes(numBytes);
+    }
+
     @Override
     public int unconsumedBytes(Http2Stream stream) {
         return state(stream).unconsumedBytes();
diff --git a/codec-http2/src/test/java/io/netty/handler/codec/http2/DefaultHttp2LocalFlowControllerTest.java b/codec-http2/src/test/java/io/netty/handler/codec/http2/DefaultHttp2LocalFlowControllerTest.java
index 104e355882..cea7793a4e 100644
--- a/codec-http2/src/test/java/io/netty/handler/codec/http2/DefaultHttp2LocalFlowControllerTest.java
+++ b/codec-http2/src/test/java/io/netty/handler/codec/http2/DefaultHttp2LocalFlowControllerTest.java
@@ -27,6 +27,7 @@ import static org.mockito.Mockito.anyInt;
 import static org.mockito.Mockito.eq;
 import static org.mockito.Mockito.never;
 import static org.mockito.Mockito.reset;
+import static org.mockito.Mockito.times;
 import static org.mockito.Mockito.verify;
 import static org.mockito.Mockito.verifyNoMoreInteractions;
 import static org.mockito.Mockito.when;
@@ -42,6 +43,8 @@ import org.junit.Before;
 import org.junit.Test;
 import org.mockito.Mock;
 import org.mockito.MockitoAnnotations;
+import org.mockito.invocation.InvocationOnMock;
+import org.mockito.stubbing.Answer;
 
 /**
  * Tests for {@link DefaultHttp2LocalFlowController}.
@@ -68,15 +71,28 @@ public class DefaultHttp2LocalFlowControllerTest {
     @Before
     public void setup() throws Http2Exception {
         MockitoAnnotations.initMocks(this);
-
-        when(ctx.newPromise()).thenReturn(promise);
-        when(ctx.flush()).thenThrow(new AssertionFailedError("forbidden"));
-        when(ctx.executor()).thenReturn(executor);
+        setupChannelHandlerContext(false);
         when(executor.inEventLoop()).thenReturn(true);
 
         initController(false);
     }
 
+    private void setupChannelHandlerContext(boolean allowFlush) {
+        reset(ctx);
+        when(ctx.newPromise()).thenReturn(promise);
+        if (allowFlush) {
+            when(ctx.flush()).then(new Answer<ChannelHandlerContext>() {
+                @Override
+                public ChannelHandlerContext answer(InvocationOnMock invocationOnMock) {
+                    return ctx;
+                }
+            });
+        } else {
+            when(ctx.flush()).thenThrow(new AssertionFailedError("forbidden"));
+        }
+        when(ctx.executor()).thenReturn(executor);
+    }
+
     @Test
     public void dataFrameShouldBeAccepted() throws Http2Exception {
         receiveFlowControlledFrame(STREAM_ID, 10, 0, false);
@@ -162,6 +178,24 @@ public class DefaultHttp2LocalFlowControllerTest {
         verifyWindowUpdateNotSent(STREAM_ID);
     }
 
+    @Test
+    public void windowUpdateShouldBeWrittenWhenStreamIsClosedAndFlushed() throws Http2Exception {
+        int dataSize = (int) (DEFAULT_WINDOW_SIZE * DEFAULT_WINDOW_UPDATE_RATIO) + 1;
+
+        setupChannelHandlerContext(true);
+
+        receiveFlowControlledFrame(STREAM_ID, dataSize, 0, false);
+        verifyWindowUpdateNotSent(CONNECTION_STREAM_ID);
+        verifyWindowUpdateNotSent(STREAM_ID);
+
+        connection.stream(STREAM_ID).close();
+
+        verifyWindowUpdateSent(CONNECTION_STREAM_ID, dataSize);
+
+        // Verify we saw one flush.
+        verify(ctx).flush();
+    }
+
     @Test
     public void halfWindowRemainingShouldUpdateAllWindows() throws Http2Exception {
         int dataSize = (int) (DEFAULT_WINDOW_SIZE * DEFAULT_WINDOW_UPDATE_RATIO) + 1;