diff --git a/server/src/main/java/org/apache/druid/segment/realtime/firehose/ChatHandlerResource.java b/server/src/main/java/org/apache/druid/segment/realtime/firehose/ChatHandlerResource.java
index 60a73153471..1cd579d2734 100644
--- a/server/src/main/java/org/apache/druid/segment/realtime/firehose/ChatHandlerResource.java
+++ b/server/src/main/java/org/apache/druid/segment/realtime/firehose/ChatHandlerResource.java
@@ -24,6 +24,7 @@ import com.google.common.collect.Iterables;
 import com.google.inject.Inject;
 import org.apache.druid.java.util.common.StringUtils;
 import org.apache.druid.server.initialization.jetty.BadRequestException;
+import org.apache.druid.server.initialization.jetty.ServiceUnavailableException;
 import org.apache.druid.server.metrics.DataSourceTaskIdHolder;
 
 import javax.ws.rs.Path;
@@ -73,6 +74,7 @@ public class ChatHandlerResource
       return handler.get();
     }
 
-    throw new BadRequestException(StringUtils.format("Can't find chatHandler for handler[%s]", handlerId));
+    // Return HTTP 503 so SpecificTaskRetryPolicy retries in case the handler is not registered yet or has been registered before shutdown.
+    throw new ServiceUnavailableException(StringUtils.format("Can't find chatHandler for handler[%s]", handlerId));
   }
 }
diff --git a/server/src/test/java/org/apache/druid/segment/realtime/firehose/ChatHandlerResourceTest.java b/server/src/test/java/org/apache/druid/segment/realtime/firehose/ChatHandlerResourceTest.java
new file mode 100644
index 00000000000..870636fb416
--- /dev/null
+++ b/server/src/test/java/org/apache/druid/segment/realtime/firehose/ChatHandlerResourceTest.java
@@ -0,0 +1,56 @@
+/*
+ * Licensed to the Apache Software Foundation (ASF) under one
+ * or more contributor license agreements.  See the NOTICE file
+ * distributed with this work for additional information
+ * regarding copyright ownership.  The ASF licenses this file
+ * to you 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 org.apache.druid.segment.realtime.firehose;
+
+import com.google.common.base.Optional;
+import org.apache.druid.server.initialization.jetty.ServiceUnavailableException;
+import org.apache.druid.server.metrics.DataSourceTaskIdHolder;
+import org.easymock.EasyMock;
+import org.easymock.EasyMockRunner;
+import org.easymock.EasyMockSupport;
+import org.easymock.Mock;
+import org.junit.Assert;
+import org.junit.Test;
+import org.junit.runner.RunWith;
+
+@RunWith(EasyMockRunner.class)
+public class ChatHandlerResourceTest extends EasyMockSupport
+{
+
+  @Mock
+  ChatHandlerProvider handlers;
+  @Mock
+  DataSourceTaskIdHolder dataSourceTaskIdHolder;
+  ChatHandlerResource chatHandlerResource;
+
+  @Test
+  public void test_noHandlerFound()
+  {
+    String handlerId = "handlerId";
+    EasyMock.expect(dataSourceTaskIdHolder.getTaskId()).andReturn(null);
+    EasyMock.expect(handlers.get(handlerId)).andReturn(Optional.absent());
+
+    replayAll();
+    chatHandlerResource = new ChatHandlerResource(handlers, dataSourceTaskIdHolder);
+    Assert.assertThrows(ServiceUnavailableException.class, () -> chatHandlerResource.doTaskChat(handlerId, null));
+    verifyAll();
+  }
+}