diff --git a/docs/changelog/126035.yaml b/docs/changelog/126035.yaml
new file mode 100644
index 000000000000..1a96205e476e
--- /dev/null
+++ b/docs/changelog/126035.yaml
@@ -0,0 +1,5 @@
+pr: 126035
+summary: Fix top level knn search with scroll
+area: Vector Search
+type: bug
+issues: []
diff --git a/server/src/internalClusterTest/java/org/elasticsearch/search/KnnSearchIT.java b/server/src/internalClusterTest/java/org/elasticsearch/search/KnnSearchIT.java
new file mode 100644
index 000000000000..91409e5e7018
--- /dev/null
+++ b/server/src/internalClusterTest/java/org/elasticsearch/search/KnnSearchIT.java
@@ -0,0 +1,137 @@
+/*
+ * Copyright Elasticsearch B.V. and/or licensed to Elasticsearch B.V. under one
+ * or more contributor license agreements. Licensed under the "Elastic License
+ * 2.0", the "GNU Affero General Public License v3.0 only", and the "Server Side
+ * Public License v 1"; you may not use this file except in compliance with, at
+ * your election, the "Elastic License 2.0", the "GNU Affero General Public
+ * License v3.0 only", or the "Server Side Public License, v 1".
+ */
+
+package org.elasticsearch.search;
+
+import org.elasticsearch.action.search.SearchRequest;
+import org.elasticsearch.action.search.SearchResponse;
+import org.elasticsearch.client.internal.Client;
+import org.elasticsearch.common.settings.Settings;
+import org.elasticsearch.core.TimeValue;
+import org.elasticsearch.index.query.QueryBuilders;
+import org.elasticsearch.search.builder.SearchSourceBuilder;
+import org.elasticsearch.search.vectors.KnnSearchBuilder;
+import org.elasticsearch.search.vectors.KnnVectorQueryBuilder;
+import org.elasticsearch.test.ESIntegTestCase;
+import org.elasticsearch.xcontent.XContentBuilder;
+import org.elasticsearch.xcontent.XContentFactory;
+
+import java.util.List;
+
+import static org.hamcrest.Matchers.notNullValue;
+
+@ESIntegTestCase.ClusterScope(minNumDataNodes = 2)
+public class KnnSearchIT extends ESIntegTestCase {
+
+    private static final String INDEX_NAME = "test_knn_index";
+    private static final String VECTOR_FIELD = "vector";
+
+    private XContentBuilder createKnnMapping() throws Exception {
+        return XContentFactory.jsonBuilder()
+            .startObject()
+            .startObject("properties")
+            .startObject(VECTOR_FIELD)
+            .field("type", "dense_vector")
+            .field("dims", 2)
+            .field("index", true)
+            .field("similarity", "l2_norm")
+            .startObject("index_options")
+            .field("type", "hnsw")
+            .endObject()
+            .endObject()
+            .startObject("category")
+            .field("type", "keyword")
+            .endObject()
+            .endObject()
+            .endObject();
+    }
+
+    public void testKnnSearchWithScroll() throws Exception {
+        final int numShards = randomIntBetween(1, 3);
+        Client client = client();
+        client.admin()
+            .indices()
+            .prepareCreate(INDEX_NAME)
+            .setSettings(Settings.builder().put("index.number_of_shards", numShards))
+            .setMapping(createKnnMapping())
+            .get();
+
+        final int count = 100;
+        for (int i = 0; i < count; i++) {
+            XContentBuilder source = XContentFactory.jsonBuilder()
+                .startObject()
+                .field(VECTOR_FIELD, new float[] { i * 0.1f, i * 0.1f })
+                .field("category", i >= 90 ? "last_ten" : null)
+                .endObject();
+            client.prepareIndex(INDEX_NAME).setSource(source).get();
+        }
+        refresh(INDEX_NAME);
+
+        final int k = randomIntBetween(11, 15);
+        // test top level knn search
+        {
+            SearchSourceBuilder sourceBuilder = new SearchSourceBuilder();
+            sourceBuilder.knnSearch(List.of(new KnnSearchBuilder(VECTOR_FIELD, new float[] { 0, 0 }, k, 100, null, null)));
+            executeScrollSearch(client, sourceBuilder, k);
+        }
+        // test top level knn search + another query
+        {
+            SearchSourceBuilder sourceBuilder = new SearchSourceBuilder();
+            sourceBuilder.knnSearch(List.of(new KnnSearchBuilder(VECTOR_FIELD, new float[] { 0, 0 }, k, 100, null, null)));
+            sourceBuilder.query(QueryBuilders.existsQuery("category").boost(10));
+            executeScrollSearch(client, sourceBuilder, k + 10);
+        }
+
+        // test knn query
+        {
+            SearchSourceBuilder sourceBuilder = new SearchSourceBuilder();
+            sourceBuilder.query(new KnnVectorQueryBuilder(VECTOR_FIELD, new float[] { 0, 0 }, k, 100, null, null));
+            executeScrollSearch(client, sourceBuilder, k * numShards);
+        }
+        // test knn query + another query
+        {
+            SearchSourceBuilder sourceBuilder = new SearchSourceBuilder();
+            sourceBuilder.query(
+                QueryBuilders.boolQuery()
+                    .should(new KnnVectorQueryBuilder(VECTOR_FIELD, new float[] { 0, 0 }, k, 100, null, null))
+                    .should(QueryBuilders.existsQuery("category").boost(10))
+            );
+            executeScrollSearch(client, sourceBuilder, k * numShards + 10);
+        }
+
+    }
+
+    private static void executeScrollSearch(Client client, SearchSourceBuilder sourceBuilder, int expectedNumHits) {
+        SearchRequest searchRequest = new SearchRequest(INDEX_NAME);
+        searchRequest.source(sourceBuilder).scroll(TimeValue.timeValueMinutes(1));
+
+        SearchResponse searchResponse = client.search(searchRequest).actionGet();
+        int hitsCollected = 0;
+        float prevScore = Float.POSITIVE_INFINITY;
+        try {
+            do {
+                assertThat(searchResponse.getScrollId(), notNullValue());
+                assertEquals(expectedNumHits, searchResponse.getHits().getTotalHits().value());
+                // assert correct order of returned hits
+                for (var searchHit : searchResponse.getHits()) {
+                    assert (searchHit.getScore() <= prevScore);
+                    prevScore = searchHit.getScore();
+                    hitsCollected += 1;
+                }
+                searchResponse.decRef();
+                searchResponse = client().prepareSearchScroll(searchResponse.getScrollId()).setScroll(TimeValue.timeValueMinutes(1)).get();
+            } while (searchResponse.getHits().getHits().length > 0);
+        } finally {
+            assertEquals(expectedNumHits, hitsCollected);
+            clearScroll(searchResponse.getScrollId());
+            searchResponse.decRef();
+        }
+    }
+
+}
diff --git a/server/src/main/java/org/elasticsearch/search/internal/LegacyReaderContext.java b/server/src/main/java/org/elasticsearch/search/internal/LegacyReaderContext.java
index e028c3739053..3d0e63868db5 100644
--- a/server/src/main/java/org/elasticsearch/search/internal/LegacyReaderContext.java
+++ b/server/src/main/java/org/elasticsearch/search/internal/LegacyReaderContext.java
@@ -72,6 +72,11 @@ public final class LegacyReaderContext extends ReaderContext {
 
     @Override
     public ShardSearchRequest getShardSearchRequest(ShardSearchRequest other) {
+        if (other != null) {
+            // The top level knn search modifies the source after the DFS phase.
+            // so we need to update the source stored in the context.
+            shardSearchRequest.source(other.source());
+        }
         return shardSearchRequest;
     }