diff --git a/modules/transport-netty4/src/main/java/org/elasticsearch/http/netty4/Netty4HttpHeaderValidator.java b/modules/transport-netty4/src/main/java/org/elasticsearch/http/netty4/Netty4HttpHeaderValidator.java
index ad322503b0d06..a07f1cc9e3386 100644
--- a/modules/transport-netty4/src/main/java/org/elasticsearch/http/netty4/Netty4HttpHeaderValidator.java
+++ b/modules/transport-netty4/src/main/java/org/elasticsearch/http/netty4/Netty4HttpHeaderValidator.java
@@ -60,6 +60,7 @@ public void channelRead(ChannelHandlerContext ctx, Object msg) throws Exception
                 pending.add(ReferenceCountUtil.retain(httpObject));
                 requestStart(ctx);
                 assert state == QUEUEING_DATA;
+                assert ctx.channel().config().isAutoRead() == false;
                 break;
             case QUEUEING_DATA:
                 pending.add(ReferenceCountUtil.retain(httpObject));
@@ -76,14 +77,14 @@ public void channelRead(ChannelHandlerContext ctx, Object msg) throws Exception
                 if (httpObject instanceof LastHttpContent) {
                     state = WAITING_TO_START;
                 }
-                // fall-through
+                ReferenceCountUtil.release(httpObject);
+                break;
             case DROPPING_DATA_PERMANENTLY:
                 assert pending.isEmpty();
                 ReferenceCountUtil.release(httpObject); // consume without enqueuing
+                ctx.channel().config().setAutoRead(false);
                 break;
         }
-
-        setAutoReadForState(ctx, state);
     }
 
     private void requestStart(ChannelHandlerContext ctx) {
@@ -104,6 +105,7 @@ private void requestStart(ChannelHandlerContext ctx) {
         }
 
         state = QUEUEING_DATA;
+        ctx.channel().config().setAutoRead(false);
 
         if (httpRequest == null) {
             // this looks like a malformed request and will forward without validation
@@ -149,6 +151,7 @@ private void forwardFullRequest(ChannelHandlerContext ctx) {
         assert ctx.channel().config().isAutoRead() == false;
         assert state == QUEUEING_DATA;
 
+        ctx.channel().config().setAutoRead(true);
         boolean fullRequestForwarded = forwardData(ctx, pending);
 
         assert fullRequestForwarded || pending.isEmpty();
@@ -160,7 +163,6 @@ private void forwardFullRequest(ChannelHandlerContext ctx) {
         }
 
         assert state == WAITING_TO_START || state == QUEUEING_DATA || state == FORWARDING_DATA_UNTIL_NEXT_REQUEST;
-        setAutoReadForState(ctx, state);
     }
 
     private void forwardRequestWithDecoderExceptionAndNoContent(ChannelHandlerContext ctx, Exception e) {
@@ -176,6 +178,8 @@ private void forwardRequestWithDecoderExceptionAndNoContent(ChannelHandlerContex
             messageToForward = toReplace.replace(Unpooled.EMPTY_BUFFER);
         }
         messageToForward.setDecoderResult(DecoderResult.failure(e));
+
+        ctx.channel().config().setAutoRead(true);
         ctx.fireChannelRead(messageToForward);
 
         assert fullRequestDropped || pending.isEmpty();
@@ -187,7 +191,6 @@ private void forwardRequestWithDecoderExceptionAndNoContent(ChannelHandlerContex
         }
 
         assert state == WAITING_TO_START || state == QUEUEING_DATA || state == DROPPING_DATA_UNTIL_NEXT_REQUEST;
-        setAutoReadForState(ctx, state);
     }
 
     @Override
@@ -243,10 +246,6 @@ private static void maybeResizePendingDown(int largeSize, ArrayDeque<HttpObject>
         }
     }
 
-    private static void setAutoReadForState(ChannelHandlerContext ctx, State state) {
-        ctx.channel().config().setAutoRead((state == QUEUEING_DATA || state == DROPPING_DATA_PERMANENTLY) == false);
-    }
-
     enum State {
         WAITING_TO_START,
         QUEUEING_DATA,
diff --git a/modules/transport-netty4/src/test/java/org/elasticsearch/http/netty4/Netty4HttpHeaderValidatorTests.java b/modules/transport-netty4/src/test/java/org/elasticsearch/http/netty4/Netty4HttpHeaderValidatorTests.java
index e8622f2c95c2c..d395a3d18e2fd 100644
--- a/modules/transport-netty4/src/test/java/org/elasticsearch/http/netty4/Netty4HttpHeaderValidatorTests.java
+++ b/modules/transport-netty4/src/test/java/org/elasticsearch/http/netty4/Netty4HttpHeaderValidatorTests.java
@@ -116,6 +116,36 @@ public void testValidationPausesAndResumesData() {
         assertThat(netty4HttpHeaderValidator.getState(), equalTo(QUEUEING_DATA));
     }
 
+    public void testValidatorDoesNotTweakAutoReadAfterValidationComplete() {
+        assertTrue(channel.config().isAutoRead());
+        assertThat(netty4HttpHeaderValidator.getState(), equalTo(WAITING_TO_START));
+
+        final DefaultHttpRequest request = new DefaultHttpRequest(HttpVersion.HTTP_1_1, HttpMethod.GET, "/uri");
+        DefaultHttpContent content = new DefaultHttpContent(Unpooled.buffer(4));
+        channel.writeInbound(request);
+        channel.writeInbound(content);
+
+        assertThat(header.get(), sameInstance(request));
+        // channel is paused
+        assertThat(channel.readInbound(), nullValue());
+        assertFalse(channel.config().isAutoRead());
+
+        // channel is resumed
+        listener.get().onResponse(null);
+        channel.runPendingTasks();
+
+        assertTrue(channel.config().isAutoRead());
+        assertThat(netty4HttpHeaderValidator.getState(), equalTo(FORWARDING_DATA_UNTIL_NEXT_REQUEST));
+        assertThat(channel.readInbound(), sameInstance(request));
+        assertThat(channel.readInbound(), sameInstance(content));
+        assertThat(channel.readInbound(), nullValue());
+        assertThat(content.refCnt(), equalTo(1));
+        channel.config().setAutoRead(false);
+
+        channel.writeOutbound(new DefaultHttpContent(Unpooled.buffer(4)));
+        assertFalse(channel.config().isAutoRead());
+    }
+
     public void testContentForwardedAfterValidation() {
         assertTrue(channel.config().isAutoRead());
         assertThat(netty4HttpHeaderValidator.getState(), equalTo(WAITING_TO_START));