diff --git a/docs/CHANGELOG.asciidoc b/docs/CHANGELOG.asciidoc
index 66a81038f0d..aa7374c2993 100644
--- a/docs/CHANGELOG.asciidoc
+++ b/docs/CHANGELOG.asciidoc
@@ -107,6 +107,7 @@ ones that the user is authorized to access in case field level security is enabl
 Fixed prerelease version of elasticsearch in the `deb` package to sort before GA versions
 ({pull}29000[#29000])
 
+Respect accept header on requests with no handler ({pull}30383[#30383])
 Rollup::
 * Validate timezone in range queries to ensure they match the selected job when
 searching ({pull}30338[#30338])
diff --git a/qa/smoke-test-http/src/test/java/org/elasticsearch/http/NoHandlerIT.java b/qa/smoke-test-http/src/test/java/org/elasticsearch/http/NoHandlerIT.java
new file mode 100644
index 00000000000..0a2d7ed9b06
--- /dev/null
+++ b/qa/smoke-test-http/src/test/java/org/elasticsearch/http/NoHandlerIT.java
@@ -0,0 +1,59 @@
+/*
+ * Licensed to Elasticsearch under one or more contributor
+ * license agreements. See the NOTICE file distributed with
+ * this work for additional information regarding copyright
+ * ownership. Elasticsearch 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.elasticsearch.http;
+
+import org.apache.http.message.BasicHeader;
+import org.apache.http.util.EntityUtils;
+import org.elasticsearch.client.Response;
+import org.elasticsearch.client.ResponseException;
+
+import java.io.IOException;
+
+import static org.hamcrest.Matchers.containsString;
+import static org.hamcrest.Matchers.equalTo;
+import static org.hamcrest.Matchers.is;
+
+public class NoHandlerIT extends HttpSmokeTestCase {
+
+    public void testNoHandlerRespectsAcceptHeader() throws IOException {
+        runTestNoHandlerRespectsAcceptHeader(
+                "application/json",
+                "application/json; charset=UTF-8",
+                "\"error\":\"no handler found for uri [/foo/bar/baz/qux/quux] and method [GET]\"");
+        runTestNoHandlerRespectsAcceptHeader(
+                "application/yaml",
+                "application/yaml",
+                "error: \"no handler found for uri [/foo/bar/baz/qux/quux] and method [GET]\"");
+    }
+
+    private void runTestNoHandlerRespectsAcceptHeader(
+            final String accept, final String contentType, final String expect) throws IOException {
+        final ResponseException e =
+                expectThrows(
+                        ResponseException.class,
+                        () -> getRestClient().performRequest("GET", "/foo/bar/baz/qux/quux", new BasicHeader("Accept", accept)));
+
+        final Response response = e.getResponse();
+        assertThat(response.getHeader("Content-Type"), equalTo(contentType));
+        assertThat(EntityUtils.toString(e.getResponse().getEntity()), containsString(expect));
+        assertThat(response.getStatusLine().getStatusCode(), is(400));
+    }
+
+}
diff --git a/server/src/main/java/org/elasticsearch/rest/RestController.java b/server/src/main/java/org/elasticsearch/rest/RestController.java
index 111663497d7..aae63f041fa 100644
--- a/server/src/main/java/org/elasticsearch/rest/RestController.java
+++ b/server/src/main/java/org/elasticsearch/rest/RestController.java
@@ -401,9 +401,15 @@ public class RestController extends AbstractComponent implements HttpServerTrans
      * Handle a requests with no candidate handlers (return a 400 Bad Request
      * error).
      */
-    private void handleBadRequest(RestRequest request, RestChannel channel) {
-        channel.sendResponse(new BytesRestResponse(BAD_REQUEST,
-            "No handler found for uri [" + request.uri() + "] and method [" + request.method() + "]"));
+    private void handleBadRequest(RestRequest request, RestChannel channel) throws IOException {
+        try (XContentBuilder builder = channel.newErrorBuilder()) {
+            builder.startObject();
+            {
+                builder.field("error", "no handler found for uri [" + request.uri() + "] and method [" + request.method() + "]");
+            }
+            builder.endObject();
+            channel.sendResponse(new BytesRestResponse(BAD_REQUEST, builder));
+        }
     }
 
     /**
diff --git a/x-pack/qa/ml-disabled/src/test/java/org/elasticsearch/xpack/ml/integration/MlPluginDisabledIT.java b/x-pack/qa/ml-disabled/src/test/java/org/elasticsearch/xpack/ml/integration/MlPluginDisabledIT.java
index e7a0a6028d4..3bb9566e5bf 100644
--- a/x-pack/qa/ml-disabled/src/test/java/org/elasticsearch/xpack/ml/integration/MlPluginDisabledIT.java
+++ b/x-pack/qa/ml-disabled/src/test/java/org/elasticsearch/xpack/ml/integration/MlPluginDisabledIT.java
@@ -51,6 +51,6 @@ public class MlPluginDisabledIT extends ESRestTestCase {
         ResponseException exception = expectThrows(ResponseException.class, () -> client().performRequest("put",
                 MachineLearning.BASE_PATH + "anomaly_detectors/foo", Collections.emptyMap(),
                         new StringEntity(Strings.toString(xContentBuilder), ContentType.APPLICATION_JSON)));
-        assertThat(exception.getMessage(), containsString("No handler found for uri [/_xpack/ml/anomaly_detectors/foo] and method [PUT]"));
+        assertThat(exception.getMessage(), containsString("no handler found for uri [/_xpack/ml/anomaly_detectors/foo] and method [PUT]"));
     }
 }