diff --git a/x-pack/plugin/core/src/main/java/org/elasticsearch/xpack/core/indexing/AsyncTwoPhaseIndexer.java b/x-pack/plugin/core/src/main/java/org/elasticsearch/xpack/core/indexing/AsyncTwoPhaseIndexer.java
index 0c4477b6b70..f9bbf890fe6 100644
--- a/x-pack/plugin/core/src/main/java/org/elasticsearch/xpack/core/indexing/AsyncTwoPhaseIndexer.java
+++ b/x-pack/plugin/core/src/main/java/org/elasticsearch/xpack/core/indexing/AsyncTwoPhaseIndexer.java
@@ -90,28 +90,21 @@ public abstract class AsyncTwoPhaseIndexer<JobPosition, JobStats extends Indexer
      * Sets the internal state to {@link IndexerState#STOPPING} if an async job is
      * running in the background, {@link #onStop()} will be called when the background job
      * detects that the indexer is stopped.
-     * If there is no job running when this function is called
-     * the state is set to {@link IndexerState#STOPPED} and {@link #onStop()} called directly.
+     * If there is no job running when this function is called the returned
+     * state is {@link IndexerState#STOPPED} and {@link #onStop()} will not be called.
      *
      * @return The new state for the indexer (STOPPED, STOPPING or ABORTING if the job was already aborted).
      */
     public synchronized IndexerState stop() {
-        AtomicBoolean wasStartedAndSetStopped = new AtomicBoolean(false);
-        IndexerState currentState = state.updateAndGet(previousState -> {
+        return state.updateAndGet(previousState -> {
             if (previousState == IndexerState.INDEXING) {
                 return IndexerState.STOPPING;
             } else if (previousState == IndexerState.STARTED) {
-                wasStartedAndSetStopped.set(true);
                 return IndexerState.STOPPED;
             } else {
                 return previousState;
             }
         });
-
-        if (wasStartedAndSetStopped.get()) {
-            onStop();
-        }
-        return currentState;
     }
 
     /**
@@ -288,20 +281,22 @@ public abstract class AsyncTwoPhaseIndexer<JobPosition, JobStats extends Indexer
     }
 
     private IndexerState finishAndSetState() {
-        return state.updateAndGet(prev -> {
+        AtomicBoolean callOnStop = new AtomicBoolean(false);
+        AtomicBoolean callOnAbort = new AtomicBoolean(false);
+        IndexerState updatedState = state.updateAndGet(prev -> {
             switch (prev) {
             case INDEXING:
                 // ready for another job
                 return IndexerState.STARTED;
 
             case STOPPING:
+                callOnStop.set(true);
                 // must be started again
-                onStop();
                 return IndexerState.STOPPED;
 
             case ABORTING:
+                callOnAbort.set(true);
                 // abort and exit
-                onAbort();
                 return IndexerState.ABORTING; // This shouldn't matter, since onAbort() will kill the task first
 
             case STOPPED:
@@ -316,6 +311,14 @@ public abstract class AsyncTwoPhaseIndexer<JobPosition, JobStats extends Indexer
                 throw new IllegalStateException("Indexer job encountered an illegal state [" + prev + "]");
             }
         });
+
+        if (callOnStop.get()) {
+            onStop();
+        } else if (callOnAbort.get()) {
+            onAbort();
+        }
+
+        return updatedState;
     }
 
     private void onSearchResponse(SearchResponse searchResponse) {
diff --git a/x-pack/plugin/core/src/test/java/org/elasticsearch/xpack/core/indexing/AsyncTwoPhaseIndexerTests.java b/x-pack/plugin/core/src/test/java/org/elasticsearch/xpack/core/indexing/AsyncTwoPhaseIndexerTests.java
index fc86a955488..053e41d9b2a 100644
--- a/x-pack/plugin/core/src/test/java/org/elasticsearch/xpack/core/indexing/AsyncTwoPhaseIndexerTests.java
+++ b/x-pack/plugin/core/src/test/java/org/elasticsearch/xpack/core/indexing/AsyncTwoPhaseIndexerTests.java
@@ -268,25 +268,6 @@ public class AsyncTwoPhaseIndexerTests extends ESTestCase {
         }
     }
 
-    public void testStop_AfterIndexerIsFinished() throws InterruptedException {
-        AtomicReference<IndexerState> state = new AtomicReference<>(IndexerState.STOPPED);
-        final ExecutorService executor = Executors.newFixedThreadPool(1);
-        try {
-            CountDownLatch countDownLatch = new CountDownLatch(1);
-            MockIndexer indexer = new MockIndexer(executor, state, 2, countDownLatch, false);
-            indexer.start();
-            assertTrue(indexer.maybeTriggerAsyncJob(System.currentTimeMillis()));
-            countDownLatch.countDown();
-            assertTrue(awaitBusy(() -> isFinished.get()));
-
-            indexer.stop();
-            assertTrue(isStopped.get());
-            assertThat(indexer.getState(), equalTo(IndexerState.STOPPED));
-        } finally {
-            executor.shutdownNow();
-        }
-    }
-
     public void testStop_WhileIndexing() throws InterruptedException {
         AtomicReference<IndexerState> state = new AtomicReference<>(IndexerState.STOPPED);
         final ExecutorService executor = Executors.newFixedThreadPool(1);
diff --git a/x-pack/plugin/data-frame/qa/multi-node-tests/src/test/java/org/elasticsearch/xpack/dataframe/integration/DataFrameTransformIT.java b/x-pack/plugin/data-frame/qa/multi-node-tests/src/test/java/org/elasticsearch/xpack/dataframe/integration/DataFrameTransformIT.java
index 1ec425c6416..69fb980871d 100644
--- a/x-pack/plugin/data-frame/qa/multi-node-tests/src/test/java/org/elasticsearch/xpack/dataframe/integration/DataFrameTransformIT.java
+++ b/x-pack/plugin/data-frame/qa/multi-node-tests/src/test/java/org/elasticsearch/xpack/dataframe/integration/DataFrameTransformIT.java
@@ -30,7 +30,6 @@ public class DataFrameTransformIT extends DataFrameIntegTestCase {
         cleanUp();
     }
 
-    @AwaitsFix( bugUrl = "https://github.com/elastic/elasticsearch/issues/42344")
     public void testDataFrameTransformCrud() throws Exception {
         createReviewsIndex();
 
diff --git a/x-pack/plugin/data-frame/qa/single-node-tests/src/test/java/org/elasticsearch/xpack/dataframe/integration/DataFrameAuditorIT.java b/x-pack/plugin/data-frame/qa/single-node-tests/src/test/java/org/elasticsearch/xpack/dataframe/integration/DataFrameAuditorIT.java
index 7dc79c1ae8f..9884c9bb679 100644
--- a/x-pack/plugin/data-frame/qa/single-node-tests/src/test/java/org/elasticsearch/xpack/dataframe/integration/DataFrameAuditorIT.java
+++ b/x-pack/plugin/data-frame/qa/single-node-tests/src/test/java/org/elasticsearch/xpack/dataframe/integration/DataFrameAuditorIT.java
@@ -6,7 +6,6 @@
 
 package org.elasticsearch.xpack.dataframe.integration;
 
-import org.apache.lucene.util.LuceneTestCase;
 import org.elasticsearch.client.Request;
 import org.elasticsearch.xpack.dataframe.persistence.DataFrameInternalIndex;
 import org.junit.Before;
@@ -23,7 +22,6 @@ import static org.hamcrest.CoreMatchers.notNullValue;
 import static org.hamcrest.Matchers.empty;
 import static org.hamcrest.Matchers.is;
 
-@LuceneTestCase.AwaitsFix( bugUrl = "https://github.com/elastic/elasticsearch/issues/42344")
 public class DataFrameAuditorIT extends DataFrameRestTestCase {
 
     private static final String TEST_USER_NAME = "df_admin_plus_data";
diff --git a/x-pack/plugin/data-frame/qa/single-node-tests/src/test/java/org/elasticsearch/xpack/dataframe/integration/DataFrameConfigurationIndexIT.java b/x-pack/plugin/data-frame/qa/single-node-tests/src/test/java/org/elasticsearch/xpack/dataframe/integration/DataFrameConfigurationIndexIT.java
index d7e12cf2bee..681599331c8 100644
--- a/x-pack/plugin/data-frame/qa/single-node-tests/src/test/java/org/elasticsearch/xpack/dataframe/integration/DataFrameConfigurationIndexIT.java
+++ b/x-pack/plugin/data-frame/qa/single-node-tests/src/test/java/org/elasticsearch/xpack/dataframe/integration/DataFrameConfigurationIndexIT.java
@@ -8,7 +8,6 @@ package org.elasticsearch.xpack.dataframe.integration;
 
 import org.apache.http.entity.ContentType;
 import org.apache.http.entity.StringEntity;
-import org.apache.lucene.util.LuceneTestCase;
 import org.elasticsearch.client.Request;
 import org.elasticsearch.client.Response;
 import org.elasticsearch.client.ResponseException;
@@ -23,7 +22,6 @@ import java.io.IOException;
 
 import static org.elasticsearch.common.xcontent.XContentFactory.jsonBuilder;
 
-@LuceneTestCase.AwaitsFix( bugUrl = "https://github.com/elastic/elasticsearch/issues/42344")
 public class DataFrameConfigurationIndexIT extends DataFrameRestTestCase {
 
     /**
diff --git a/x-pack/plugin/data-frame/qa/single-node-tests/src/test/java/org/elasticsearch/xpack/dataframe/integration/DataFrameGetAndGetStatsIT.java b/x-pack/plugin/data-frame/qa/single-node-tests/src/test/java/org/elasticsearch/xpack/dataframe/integration/DataFrameGetAndGetStatsIT.java
index 9bac6ca0b40..d9927cd09ed 100644
--- a/x-pack/plugin/data-frame/qa/single-node-tests/src/test/java/org/elasticsearch/xpack/dataframe/integration/DataFrameGetAndGetStatsIT.java
+++ b/x-pack/plugin/data-frame/qa/single-node-tests/src/test/java/org/elasticsearch/xpack/dataframe/integration/DataFrameGetAndGetStatsIT.java
@@ -6,7 +6,6 @@
 
 package org.elasticsearch.xpack.dataframe.integration;
 
-import org.apache.lucene.util.LuceneTestCase;
 import org.elasticsearch.client.Request;
 import org.elasticsearch.common.xcontent.support.XContentMapValues;
 import org.elasticsearch.xpack.core.dataframe.DataFrameField;
@@ -22,7 +21,6 @@ import static org.elasticsearch.xpack.core.security.authc.support.UsernamePasswo
 import static org.hamcrest.Matchers.equalTo;
 import static org.hamcrest.Matchers.greaterThan;
 
-@LuceneTestCase.AwaitsFix( bugUrl = "https://github.com/elastic/elasticsearch/issues/42344")
 public class DataFrameGetAndGetStatsIT extends DataFrameRestTestCase {
 
     private static final String TEST_USER_NAME = "df_user";
diff --git a/x-pack/plugin/data-frame/qa/single-node-tests/src/test/java/org/elasticsearch/xpack/dataframe/integration/DataFrameMetaDataIT.java b/x-pack/plugin/data-frame/qa/single-node-tests/src/test/java/org/elasticsearch/xpack/dataframe/integration/DataFrameMetaDataIT.java
index 5b95d1daead..26a957ea055 100644
--- a/x-pack/plugin/data-frame/qa/single-node-tests/src/test/java/org/elasticsearch/xpack/dataframe/integration/DataFrameMetaDataIT.java
+++ b/x-pack/plugin/data-frame/qa/single-node-tests/src/test/java/org/elasticsearch/xpack/dataframe/integration/DataFrameMetaDataIT.java
@@ -6,7 +6,6 @@
 
 package org.elasticsearch.xpack.dataframe.integration;
 
-import org.apache.lucene.util.LuceneTestCase;
 import org.elasticsearch.Version;
 import org.elasticsearch.client.Request;
 import org.elasticsearch.client.Response;
@@ -16,7 +15,6 @@ import org.junit.Before;
 import java.io.IOException;
 import java.util.Map;
 
-@LuceneTestCase.AwaitsFix( bugUrl = "https://github.com/elastic/elasticsearch/issues/42344")
 public class DataFrameMetaDataIT extends DataFrameRestTestCase {
 
     private boolean indicesCreated = false;
diff --git a/x-pack/plugin/data-frame/qa/single-node-tests/src/test/java/org/elasticsearch/xpack/dataframe/integration/DataFramePivotRestIT.java b/x-pack/plugin/data-frame/qa/single-node-tests/src/test/java/org/elasticsearch/xpack/dataframe/integration/DataFramePivotRestIT.java
index 36f95e599ff..933fcc6c8e5 100644
--- a/x-pack/plugin/data-frame/qa/single-node-tests/src/test/java/org/elasticsearch/xpack/dataframe/integration/DataFramePivotRestIT.java
+++ b/x-pack/plugin/data-frame/qa/single-node-tests/src/test/java/org/elasticsearch/xpack/dataframe/integration/DataFramePivotRestIT.java
@@ -6,7 +6,6 @@
 
 package org.elasticsearch.xpack.dataframe.integration;
 
-import org.apache.lucene.util.LuceneTestCase;
 import org.elasticsearch.client.Request;
 import org.elasticsearch.common.xcontent.support.XContentMapValues;
 import org.junit.Before;
@@ -22,7 +21,6 @@ import static org.elasticsearch.xpack.core.security.authc.support.UsernamePasswo
 import static org.hamcrest.Matchers.containsString;
 import static org.hamcrest.Matchers.equalTo;
 
-@LuceneTestCase.AwaitsFix( bugUrl = "https://github.com/elastic/elasticsearch/issues/42344")
 public class DataFramePivotRestIT extends DataFrameRestTestCase {
 
     private static final String TEST_USER_NAME = "df_admin_plus_data";
diff --git a/x-pack/plugin/data-frame/qa/single-node-tests/src/test/java/org/elasticsearch/xpack/dataframe/integration/DataFrameTaskFailedStateIT.java b/x-pack/plugin/data-frame/qa/single-node-tests/src/test/java/org/elasticsearch/xpack/dataframe/integration/DataFrameTaskFailedStateIT.java
index 7b63644dd34..96aeeda8755 100644
--- a/x-pack/plugin/data-frame/qa/single-node-tests/src/test/java/org/elasticsearch/xpack/dataframe/integration/DataFrameTaskFailedStateIT.java
+++ b/x-pack/plugin/data-frame/qa/single-node-tests/src/test/java/org/elasticsearch/xpack/dataframe/integration/DataFrameTaskFailedStateIT.java
@@ -6,7 +6,6 @@
 
 package org.elasticsearch.xpack.dataframe.integration;
 
-import org.apache.lucene.util.LuceneTestCase;
 import org.elasticsearch.client.ResponseException;
 import org.elasticsearch.common.xcontent.support.XContentMapValues;
 import org.elasticsearch.rest.RestStatus;
@@ -20,7 +19,6 @@ import static org.hamcrest.CoreMatchers.is;
 import static org.hamcrest.CoreMatchers.nullValue;
 import static org.hamcrest.Matchers.equalTo;
 
-@LuceneTestCase.AwaitsFix( bugUrl = "https://github.com/elastic/elasticsearch/issues/42344")
 public class DataFrameTaskFailedStateIT extends DataFrameRestTestCase {
 
     public void testDummy() {
diff --git a/x-pack/plugin/data-frame/qa/single-node-tests/src/test/java/org/elasticsearch/xpack/dataframe/integration/DataFrameUsageIT.java b/x-pack/plugin/data-frame/qa/single-node-tests/src/test/java/org/elasticsearch/xpack/dataframe/integration/DataFrameUsageIT.java
index f98fa6a2713..4f209c5a9f3 100644
--- a/x-pack/plugin/data-frame/qa/single-node-tests/src/test/java/org/elasticsearch/xpack/dataframe/integration/DataFrameUsageIT.java
+++ b/x-pack/plugin/data-frame/qa/single-node-tests/src/test/java/org/elasticsearch/xpack/dataframe/integration/DataFrameUsageIT.java
@@ -6,7 +6,6 @@
 
 package org.elasticsearch.xpack.dataframe.integration;
 
-import org.apache.lucene.util.LuceneTestCase;
 import org.elasticsearch.client.Request;
 import org.elasticsearch.client.Response;
 import org.elasticsearch.common.xcontent.support.XContentMapValues;
@@ -23,7 +22,6 @@ import java.util.Map;
 import static org.elasticsearch.xpack.core.dataframe.DataFrameField.INDEX_DOC_TYPE;
 import static org.elasticsearch.xpack.dataframe.DataFrameFeatureSet.PROVIDED_STATS;
 
-@LuceneTestCase.AwaitsFix( bugUrl = "https://github.com/elastic/elasticsearch/issues/42344")
 public class DataFrameUsageIT extends DataFrameRestTestCase {
     private boolean indicesCreated = false;
 
diff --git a/x-pack/plugin/data-frame/src/main/java/org/elasticsearch/xpack/dataframe/transforms/DataFrameTransformTask.java b/x-pack/plugin/data-frame/src/main/java/org/elasticsearch/xpack/dataframe/transforms/DataFrameTransformTask.java
index 13deab6748c..575cd4c15bd 100644
--- a/x-pack/plugin/data-frame/src/main/java/org/elasticsearch/xpack/dataframe/transforms/DataFrameTransformTask.java
+++ b/x-pack/plugin/data-frame/src/main/java/org/elasticsearch/xpack/dataframe/transforms/DataFrameTransformTask.java
@@ -66,7 +66,7 @@ public class DataFrameTransformTask extends AllocatedPersistentTask implements S
     private final Map<String, Object> initialPosition;
     private final IndexerState initialIndexerState;
 
-    private final SetOnce<DataFrameIndexer> indexer = new SetOnce<>();
+    private final SetOnce<ClientDataFrameIndexer> indexer = new SetOnce<>();
 
     private final AtomicReference<DataFrameTransformTaskState> taskState;
     private final AtomicReference<String> stateReason;
@@ -125,7 +125,7 @@ public class DataFrameTransformTask extends AllocatedPersistentTask implements S
         return getState();
     }
 
-    private DataFrameIndexer getIndexer() {
+    private ClientDataFrameIndexer getIndexer() {
         return indexer.get();
     }
 
@@ -236,7 +236,10 @@ public class DataFrameTransformTask extends AllocatedPersistentTask implements S
             return;
         }
 
-        getIndexer().stop();
+        IndexerState state = getIndexer().stop();
+        if (state == IndexerState.STOPPED) {
+            getIndexer().doSaveState(state, getIndexer().getPosition(), () -> getIndexer().onStop());
+        }
     }
 
     @Override
@@ -530,11 +533,17 @@ public class DataFrameTransformTask extends AllocatedPersistentTask implements S
                 next.run();
                 return;
             }
+            // If we are `STOPPED` on a `doSaveState` call, that indicates we transitioned to `STOPPED` from `STOPPING`
+            // OR we called `doSaveState` manually as the indexer was not actively running.
+            // Since we save the state to an index, we should make sure that our task state is in parity with the indexer state
+            if (indexerState.equals(IndexerState.STOPPED)) {
+                transformTask.setTaskStateStopped();
+            }
 
             final DataFrameTransformState state = new DataFrameTransformState(
                 transformTask.taskState.get(),
                 indexerState,
-                getPosition(),
+                position,
                 transformTask.currentCheckpoint.get(),
                 transformTask.stateReason.get(),
                 getProgress());
@@ -542,28 +551,18 @@ public class DataFrameTransformTask extends AllocatedPersistentTask implements S
 
             // Persisting stats when we call `doSaveState` should be ok as we only call it on a state transition and
             // only every-so-often when doing the bulk indexing calls.  See AsyncTwoPhaseIndexer#onBulkResponse for current periodicity
-            ActionListener<PersistentTasksCustomMetaData.PersistentTask<?>> updateClusterStateListener = ActionListener.wrap(
-                task -> {
-                    transformsConfigManager.putOrUpdateTransformStats(
-                            new DataFrameTransformStateAndStats(transformId, state, getStats(),
-                                    DataFrameTransformCheckpointingInfo.EMPTY), // TODO should this be null
-                            ActionListener.wrap(
-                                    r -> {
-                                        next.run();
-                                    },
-                                    statsExc -> {
-                                        logger.error("Updating stats of transform [" + transformConfig.getId() + "] failed", statsExc);
-                                        next.run();
-                                    }
-                            ));
-                },
-                exc -> {
-                    logger.error("Updating persistent state of transform [" + transformConfig.getId() + "] failed", exc);
-                    next.run();
-                }
-            );
-
-            transformTask.persistStateToClusterState(state, updateClusterStateListener);
+            transformsConfigManager.putOrUpdateTransformStats(
+                    new DataFrameTransformStateAndStats(transformId, state, getStats(),
+                            DataFrameTransformCheckpointingInfo.EMPTY), // TODO should this be null
+                    ActionListener.wrap(
+                            r -> {
+                                next.run();
+                            },
+                            statsExc -> {
+                                logger.error("Updating stats of transform [" + transformConfig.getId() + "] failed", statsExc);
+                                next.run();
+                            }
+                    ));
         }
 
         @Override
@@ -602,20 +601,7 @@ public class DataFrameTransformTask extends AllocatedPersistentTask implements S
         protected void onStop() {
             auditor.info(transformConfig.getId(), "Indexer has stopped");
             logger.info("Data frame transform [{}] indexer has stopped", transformConfig.getId());
-
-            transformTask.setTaskStateStopped();
-            transformsConfigManager.putOrUpdateTransformStats(
-                    new DataFrameTransformStateAndStats(transformId, transformTask.getState(), getStats(),
-                            DataFrameTransformCheckpointingInfo.EMPTY), // TODO should this be null
-                    ActionListener.wrap(
-                            r -> {
-                                transformTask.shutdown();
-                            },
-                            statsExc -> {
-                                transformTask.shutdown();
-                                logger.error("Updating saving stats of transform [" + transformConfig.getId() + "] failed", statsExc);
-                            }
-                    ));
+            transformTask.shutdown();
         }
 
         @Override
diff --git a/x-pack/plugin/src/test/resources/rest-api-spec/test/data_frame/transforms_start_stop.yml b/x-pack/plugin/src/test/resources/rest-api-spec/test/data_frame/transforms_start_stop.yml
index 31f80033e7b..2686c57fd06 100644
--- a/x-pack/plugin/src/test/resources/rest-api-spec/test/data_frame/transforms_start_stop.yml
+++ b/x-pack/plugin/src/test/resources/rest-api-spec/test/data_frame/transforms_start_stop.yml
@@ -190,8 +190,10 @@ teardown:
   - do:
       data_frame.stop_data_frame_transform:
         transform_id: "airline-transform-start-stop"
+        wait_for_completion: true
   - match: { acknowledged: true }
 
+
   - do:
       data_frame.get_data_frame_transform_stats:
         transform_id: "airline-transform-start-later"
@@ -209,3 +211,46 @@ teardown:
   - do:
       data_frame.delete_data_frame_transform:
         transform_id: "airline-transform-start-later"
+
+---
+"Test stop all":
+  - do:
+      data_frame.put_data_frame_transform:
+        transform_id: "airline-transform-stop-all"
+        body: >
+          {
+            "source": { "index": "airline-data" },
+            "dest": { "index": "airline-data-start-later" },
+            "pivot": {
+              "group_by": { "airline": {"terms": {"field": "airline"}}},
+              "aggs": {"avg_response": {"avg": {"field": "responsetime"}}}
+            }
+          }
+  - do:
+      data_frame.start_data_frame_transform:
+        transform_id: "airline-transform-stop-all"
+  - match: { acknowledged: true }
+
+  - do:
+      data_frame.start_data_frame_transform:
+        transform_id: "airline-transform-start-stop"
+  - match: { acknowledged: true }
+
+  - do:
+      data_frame.stop_data_frame_transform:
+        transform_id: "_all"
+        wait_for_completion: true
+  - match: { acknowledged: true }
+
+  - do:
+      data_frame.get_data_frame_transform_stats:
+        transform_id: "*"
+  - match: { count: 2 }
+  - match: { transforms.0.state.indexer_state: "stopped" }
+  - match: { transforms.0.state.task_state: "stopped" }
+  - match: { transforms.1.state.indexer_state: "stopped" }
+  - match: { transforms.1.state.task_state: "stopped" }
+
+  - do:
+      data_frame.delete_data_frame_transform:
+        transform_id: "airline-transform-stop-all"