diff --git a/server/src/main/java/org/elasticsearch/search/SearchService.java b/server/src/main/java/org/elasticsearch/search/SearchService.java
index e61d507279029..ac8bbf48dff0b 100644
--- a/server/src/main/java/org/elasticsearch/search/SearchService.java
+++ b/server/src/main/java/org/elasticsearch/search/SearchService.java
@@ -634,6 +634,9 @@ final SearchContext createAndPutContext(ShardSearchRequest request, SearchShardT
         boolean success = false;
         try {
             putContext(context);
+            // ensure that if we race against afterIndexRemoved, we free the context here.
+            // this is important to ensure store can be cleaned up, in particular if the search is a scroll with a long timeout.
+            indicesService.indexServiceSafe(request.shardId().getIndex());
             success = true;
             return context;
         } finally {
diff --git a/server/src/test/java/org/elasticsearch/search/SearchServiceTests.java b/server/src/test/java/org/elasticsearch/search/SearchServiceTests.java
index 5af595026d003..8cd1a016e49ec 100644
--- a/server/src/test/java/org/elasticsearch/search/SearchServiceTests.java
+++ b/server/src/test/java/org/elasticsearch/search/SearchServiceTests.java
@@ -46,6 +46,7 @@
 import org.elasticsearch.common.xcontent.XContentBuilder;
 import org.elasticsearch.index.Index;
 import org.elasticsearch.index.IndexModule;
+import org.elasticsearch.index.IndexNotFoundException;
 import org.elasticsearch.index.IndexService;
 import org.elasticsearch.index.IndexSettings;
 import org.elasticsearch.index.query.AbstractQueryBuilder;
@@ -122,7 +123,7 @@ protected boolean resetNodeAfterTest() {
     @Override
     protected Collection<Class<? extends Plugin>> getPlugins() {
         return pluginList(FailOnRewriteQueryPlugin.class, CustomScriptPlugin.class,
-            ReaderWrapperCountPlugin.class, InternalOrPrivateSettingsPlugin.class);
+            ReaderWrapperCountPlugin.class, InternalOrPrivateSettingsPlugin.class, MockSearchService.TestPlugin.class);
     }
 
     public static class ReaderWrapperCountPlugin extends Plugin {
@@ -329,6 +330,7 @@ public void onFailure(Exception e) {
                         service.executeFetchPhase(req, new SearchShardTask(123L, "", "", "", null, Collections.emptyMap()), listener);
                         listener.get();
                         if (useScroll) {
+                            // have to free context since this test does not remove the index from IndicesService.
                             service.freeContext(searchPhaseResult.getContextId());
                         }
                     } catch (ExecutionException ex) {
@@ -357,6 +359,53 @@ public void onFailure(Exception e) {
         assertEquals(0, totalStats.getFetchCurrent());
     }
 
+    public void testSearchWhileIndexDeletedDoesNotLeakSearchContext() throws ExecutionException, InterruptedException {
+        createIndex("index");
+        client().prepareIndex("index", "type", "1").setSource("field", "value").setRefreshPolicy(IMMEDIATE).get();
+
+        IndicesService indicesService = getInstanceFromNode(IndicesService.class);
+        IndexService indexService = indicesService.indexServiceSafe(resolveIndex("index"));
+        IndexShard indexShard = indexService.getShard(0);
+
+        MockSearchService service = (MockSearchService) getInstanceFromNode(SearchService.class);
+        service.setOnPutContext(
+            context -> {
+                if (context.indexShard() == indexShard) {
+                    assertAcked(client().admin().indices().prepareDelete("index"));
+                }
+            }
+        );
+
+        SearchRequest searchRequest = new SearchRequest().allowPartialSearchResults(true);
+        SearchRequest scrollSearchRequest = new SearchRequest().allowPartialSearchResults(true)
+            .scroll(new Scroll(TimeValue.timeValueMinutes(1)));
+
+        // the scrolls are not explicitly freed, but should all be gone when the test finished.
+        // for completeness, we also randomly test the regular search path.
+        final boolean useScroll = randomBoolean();
+        PlainActionFuture<SearchPhaseResult> result = new PlainActionFuture<>();
+        service.executeQueryPhase(
+            new ShardSearchRequest(OriginalIndices.NONE, useScroll ? scrollSearchRequest : searchRequest,
+                new ShardId(resolveIndex("index"), 0), 1,
+                new AliasFilter(null, Strings.EMPTY_ARRAY), 1.0f, -1, null, null),
+            new SearchShardTask(123L, "", "", "", null, Collections.emptyMap()), result);
+
+        try {
+            result.get();
+        } catch (Exception e) {
+            // ok
+        }
+
+        expectThrows(IndexNotFoundException.class, () -> client().admin().indices().prepareGetIndex().setIndices("index").get());
+
+        assertEquals(0, service.getActiveContexts());
+
+        SearchStats.Stats totalStats = indexShard.searchStats().getTotal();
+        assertEquals(0, totalStats.getQueryCurrent());
+        assertEquals(0, totalStats.getScrollCurrent());
+        assertEquals(0, totalStats.getFetchCurrent());
+    }
+
     public void testTimeout() throws IOException {
         createIndex("index");
         final SearchService service = getInstanceFromNode(SearchService.class);
@@ -527,6 +576,8 @@ public void testMaxOpenScrollContexts() throws RuntimeException {
                 SearchService.MAX_OPEN_SCROLL_CONTEXT.get(Settings.EMPTY) + "]. " +
                 "This limit can be set by changing the [search.max_open_scroll_context] setting.",
             ex.getMessage());
+
+        service.freeAllScrollContexts();
     }
 
     public void testOpenScrollContextsConcurrently() throws Exception {
diff --git a/test/framework/src/main/java/org/elasticsearch/search/MockSearchService.java b/test/framework/src/main/java/org/elasticsearch/search/MockSearchService.java
index 9653f3b66a515..68bafed5fd4cf 100644
--- a/test/framework/src/main/java/org/elasticsearch/search/MockSearchService.java
+++ b/test/framework/src/main/java/org/elasticsearch/search/MockSearchService.java
@@ -33,6 +33,7 @@
 import java.util.HashMap;
 import java.util.Map;
 import java.util.concurrent.ConcurrentHashMap;
+import java.util.function.Consumer;
 
 public class MockSearchService extends SearchService {
     /**
@@ -42,6 +43,8 @@ public static class TestPlugin extends Plugin {}
 
     private static final Map<SearchContext, Throwable> ACTIVE_SEARCH_CONTEXTS = new ConcurrentHashMap<>();
 
+    private Consumer<SearchContext> onPutContext = context -> {};
+
     /** Throw an {@link AssertionError} if there are still in-flight contexts. */
     public static void assertNoInFlightContext() {
         final Map<SearchContext, Throwable> copy = new HashMap<>(ACTIVE_SEARCH_CONTEXTS);
@@ -75,6 +78,7 @@ public MockSearchService(ClusterService clusterService,
 
     @Override
     protected void putContext(SearchContext context) {
+        onPutContext.accept(context);
         addActiveContext(context);
         super.putContext(context);
     }
@@ -87,4 +91,8 @@ protected SearchContext removeContext(long id) {
         }
         return removed;
     }
+
+    public void setOnPutContext(Consumer<SearchContext> onPutContext) {
+        this.onPutContext = onPutContext;
+    }
 }