diff --git a/modules/runner/src/integrationTest/java/org/apache/ignite/internal/runner/app/client/ItThinClientSqlTest.java b/modules/runner/src/integrationTest/java/org/apache/ignite/internal/runner/app/client/ItThinClientSqlTest.java
index 60b14cb3ba9..0b2a21923c6 100644
--- a/modules/runner/src/integrationTest/java/org/apache/ignite/internal/runner/app/client/ItThinClientSqlTest.java
+++ b/modules/runner/src/integrationTest/java/org/apache/ignite/internal/runner/app/client/ItThinClientSqlTest.java
@@ -18,6 +18,7 @@
 package org.apache.ignite.internal.runner.app.client;
 
 import static org.apache.ignite.internal.testframework.IgniteTestUtils.await;
+import static org.apache.ignite.internal.tx.impl.ResourceVacuumManager.RESOURCE_VACUUM_INTERVAL_MILLISECONDS_PROPERTY;
 import static org.hamcrest.MatcherAssert.assertThat;
 import static org.hamcrest.Matchers.empty;
 import static org.hamcrest.Matchers.is;
@@ -31,6 +32,7 @@
 import static org.junit.jupiter.api.Assertions.assertTrue;
 
 import java.math.BigDecimal;
+import java.time.Duration;
 import java.time.LocalDate;
 import java.time.LocalDateTime;
 import java.time.LocalTime;
@@ -38,6 +40,7 @@
 import java.util.ArrayList;
 import java.util.EnumSet;
 import java.util.List;
+import java.util.Map;
 import java.util.Set;
 import java.util.UUID;
 import java.util.concurrent.CompletionException;
@@ -51,6 +54,7 @@
 import org.apache.ignite.internal.client.sql.QueryModifier;
 import org.apache.ignite.internal.security.authentication.UserDetails;
 import org.apache.ignite.internal.testframework.IgniteTestUtils;
+import org.apache.ignite.internal.testframework.WithSystemProperty;
 import org.apache.ignite.internal.tx.TxManager;
 import org.apache.ignite.internal.tx.impl.TransactionInflights;
 import org.apache.ignite.lang.IgniteException;
@@ -73,7 +77,6 @@
 import org.awaitility.Awaitility;
 import org.hamcrest.Matchers;
 import org.junit.jupiter.api.AfterEach;
-import org.junit.jupiter.api.Disabled;
 import org.junit.jupiter.api.Test;
 import org.junit.jupiter.params.ParameterizedTest;
 import org.junit.jupiter.params.provider.ValueSource;
@@ -81,6 +84,7 @@
 /**
  * Thin client SQL integration test.
  */
+@WithSystemProperty(key = RESOURCE_VACUUM_INTERVAL_MILLISECONDS_PROPERTY, value = "10")
 @SuppressWarnings("resource")
 public class ItThinClientSqlTest extends ItAbstractThinClientTest {
     @AfterEach
@@ -840,7 +844,6 @@ public void testSqlQueryModifiers() {
     }
 
     @Test
-    @Disabled("https://issues.apache.org/jira/browse/IGNITE-26567")
     public void testBroadcastQueryTxInflightStateCleanup() {
         IgniteSql sql = client().sql();
 
@@ -858,7 +861,11 @@ public void testBroadcastQueryTxInflightStateCleanup() {
             IgniteImpl server = TestWrappers.unwrapIgniteImpl(server(i));
             TxManager txManager = server.txManager();
             TransactionInflights transactionInflights = IgniteTestUtils.getFieldValue(txManager, "transactionInflights");
-            assertFalse(transactionInflights.hasActiveInflights(), "Expecting no active inflights");
+            Map<UUID, ?> txContexts = IgniteTestUtils.getFieldValue(transactionInflights, "txCtxMap");
+
+            Awaitility.await()
+                    .atMost(Duration.ofSeconds(10))
+                    .untilAsserted(() -> assertTrue(txContexts.isEmpty(), "Expecting no transaction inflight contexts"));
         }
     }
 
diff --git a/modules/transactions/src/main/java/org/apache/ignite/internal/tx/impl/FinishedTransactionBatchRequestHandler.java b/modules/transactions/src/main/java/org/apache/ignite/internal/tx/impl/FinishedTransactionBatchRequestHandler.java
index 6e265624939..171707c098c 100644
--- a/modules/transactions/src/main/java/org/apache/ignite/internal/tx/impl/FinishedTransactionBatchRequestHandler.java
+++ b/modules/transactions/src/main/java/org/apache/ignite/internal/tx/impl/FinishedTransactionBatchRequestHandler.java
@@ -34,6 +34,9 @@ public class FinishedTransactionBatchRequestHandler {
     /** Resources registry. */
     private final RemotelyTriggeredResourceRegistry resourcesRegistry;
 
+    /** Transaction inflights tracker. */
+    private final TransactionInflights transactionInflights;
+
     private final LowWatermark lowWatermark;
 
     private final Executor asyncExecutor;
@@ -43,17 +46,20 @@ public class FinishedTransactionBatchRequestHandler {
      *
      * @param messagingService Messaging service.
      * @param resourcesRegistry Resources registry.
+     * @param transactionInflights Transaction inflights.
      * @param lowWatermark Low watermark.
      * @param asyncExecutor Executor to run cleanup commands.
      */
     public FinishedTransactionBatchRequestHandler(
             MessagingService messagingService,
             RemotelyTriggeredResourceRegistry resourcesRegistry,
+            TransactionInflights transactionInflights,
             LowWatermark lowWatermark,
             Executor asyncExecutor
     ) {
         this.messagingService = messagingService;
         this.resourcesRegistry = resourcesRegistry;
+        this.transactionInflights = transactionInflights;
         this.lowWatermark = lowWatermark;
         this.asyncExecutor = asyncExecutor;
     }
@@ -74,6 +80,8 @@ private void processFinishedTransactionsBatchMessage(FinishedTransactionsBatchMe
     }
 
     private void cleanUpForTransaction(UUID transactionId) {
+        transactionInflights.removeTxContext(transactionId);
+
         resourcesRegistry.close(transactionId);
 
         lowWatermark.unlock(transactionId);
diff --git a/modules/transactions/src/main/java/org/apache/ignite/internal/tx/impl/ResourceVacuumManager.java b/modules/transactions/src/main/java/org/apache/ignite/internal/tx/impl/ResourceVacuumManager.java
index a76cc3fa43a..bcbaaf9fc0b 100644
--- a/modules/transactions/src/main/java/org/apache/ignite/internal/tx/impl/ResourceVacuumManager.java
+++ b/modules/transactions/src/main/java/org/apache/ignite/internal/tx/impl/ResourceVacuumManager.java
@@ -124,6 +124,7 @@ public ResourceVacuumManager(
         this.finishedTransactionBatchRequestHandler = new FinishedTransactionBatchRequestHandler(
                 messagingService,
                 resourceRegistry,
+                transactionInflights,
                 lowWatermark,
                 resourceVacuumExecutor
         );
diff --git a/modules/transactions/src/test/java/org/apache/ignite/internal/tx/impl/FinishedTransactionBatchRequestHandlerTest.java b/modules/transactions/src/test/java/org/apache/ignite/internal/tx/impl/FinishedTransactionBatchRequestHandlerTest.java
index ba1ba7cc25a..e879d0b6b83 100644
--- a/modules/transactions/src/test/java/org/apache/ignite/internal/tx/impl/FinishedTransactionBatchRequestHandlerTest.java
+++ b/modules/transactions/src/test/java/org/apache/ignite/internal/tx/impl/FinishedTransactionBatchRequestHandlerTest.java
@@ -54,6 +54,9 @@ class FinishedTransactionBatchRequestHandlerTest extends BaseIgniteAbstractTest
     @Mock
     private LowWatermark lowWatermark;
 
+    @Mock
+    private TransactionInflights transactionInflights;
+
     private FinishedTransactionBatchRequestHandler requestHandler;
 
     private NetworkMessageHandler networkHandler;
@@ -63,6 +66,7 @@ void createAndStartHandler() {
         requestHandler = new FinishedTransactionBatchRequestHandler(
                 messagingService,
                 resourceRegistry,
+                transactionInflights,
                 lowWatermark,
                 ForkJoinPool.commonPool()
         );
@@ -86,6 +90,8 @@ void unlocksLwm() {
 
         networkHandler.onReceived(message, mock(InternalClusterNode.class), null);
 
+        verify(transactionInflights, timeout(10_000)).removeTxContext(txId1);
+        verify(transactionInflights, timeout(10_000)).removeTxContext(txId2);
         verify(lowWatermark, timeout(10_000)).unlock(txId1);
         verify(lowWatermark, timeout(10_000)).unlock(txId2);
     }