diff --git a/sql/core/src/main/scala/org/apache/spark/sql/execution/streaming/checkpointing/ChecksumCheckpointFileManager.scala b/sql/core/src/main/scala/org/apache/spark/sql/execution/streaming/checkpointing/ChecksumCheckpointFileManager.scala
index 637d11ad890bf..2de429ee10763 100644
--- a/sql/core/src/main/scala/org/apache/spark/sql/execution/streaming/checkpointing/ChecksumCheckpointFileManager.scala
+++ b/sql/core/src/main/scala/org/apache/spark/sql/execution/streaming/checkpointing/ChecksumCheckpointFileManager.scala
@@ -39,6 +39,7 @@ import org.apache.spark.internal.LogKeys.{CHECKSUM, NUM_BYTES, PATH, TIMEOUT}
 import org.apache.spark.sql.errors.QueryExecutionErrors
 import org.apache.spark.sql.execution.streaming.checkpointing.CheckpointFileManager.CancellableFSDataOutputStream
 import org.apache.spark.util.ThreadUtils
+import org.apache.spark.util.Utils
 
 /** Information about the creator of the checksum file. Useful for debugging */
 case class ChecksumFileCreatorInfo(
@@ -500,16 +501,14 @@ class ChecksumCancellableFSDataOutputStream(
   @volatile private var closed = false
 
   override def cancel(): Unit = {
-    val mainFuture = Future {
+    // Cancel both streams synchronously rather than using futures. If the current thread is
+    // interrupted and we call this method, scheduling work on futures would immediately throw
+    // InterruptedException leaving the streams in an inconsistent state.
+    Utils.tryWithSafeFinally {
       mainStream.cancel()
-    }(uploadThreadPool)
-
-    val checksumFuture = Future {
+    } {
       checksumStream.cancel()
-    }(uploadThreadPool)
-
-    awaitResult(mainFuture, Duration.Inf)
-    awaitResult(checksumFuture, Duration.Inf)
+    }
   }
 
   override def close(): Unit = {
diff --git a/sql/core/src/main/scala/org/apache/spark/sql/execution/streaming/state/RocksDB.scala b/sql/core/src/main/scala/org/apache/spark/sql/execution/streaming/state/RocksDB.scala
index 8a2ed6d9a529d..c92c5017cada9 100644
--- a/sql/core/src/main/scala/org/apache/spark/sql/execution/streaming/state/RocksDB.scala
+++ b/sql/core/src/main/scala/org/apache/spark/sql/execution/streaming/state/RocksDB.scala
@@ -1650,17 +1650,23 @@ class RocksDB(
    * Drop uncommitted changes, and roll back to previous version.
    */
   def rollback(): Unit = {
-    numKeysOnWritingVersion = numKeysOnLoadedVersion
-    numInternalKeysOnWritingVersion = numInternalKeysOnLoadedVersion
-    loadedVersion = -1L
-    lastCommitBasedStateStoreCkptId = None
-    lastCommittedStateStoreCkptId = None
-    loadedStateStoreCkptId = None
-    sessionStateStoreCkptId = None
-    lineageManager.clear()
-    changelogWriter.foreach(_.abort())
-    // Make sure changelogWriter gets recreated next time.
-    changelogWriter = None
+    logInfo(
+      log"Rolling back uncommitted changes on version ${MDC(LogKeys.VERSION_NUM, loadedVersion)}")
+    try {
+      numKeysOnWritingVersion = numKeysOnLoadedVersion
+      numInternalKeysOnWritingVersion = numInternalKeysOnLoadedVersion
+      loadedVersion = -1L
+      lastCommitBasedStateStoreCkptId = None
+      lastCommittedStateStoreCkptId = None
+      loadedStateStoreCkptId = None
+      sessionStateStoreCkptId = None
+      lineageManager.clear()
+      changelogWriter.foreach(_.abort())
+    } finally {
+      // Make sure changelogWriter gets recreated next time even if the changelogWriter aborts with
+      // an exception.
+      changelogWriter = None
+    }
     logInfo(log"Rolled back to ${MDC(LogKeys.VERSION_NUM, loadedVersion)}")
   }
 
diff --git a/sql/core/src/test/scala/org/apache/spark/sql/execution/streaming/state/RocksDBCheckpointFailureInjectionSuite.scala b/sql/core/src/test/scala/org/apache/spark/sql/execution/streaming/state/RocksDBCheckpointFailureInjectionSuite.scala
index 0b9690ee72775..c48b492e27c27 100644
--- a/sql/core/src/test/scala/org/apache/spark/sql/execution/streaming/state/RocksDBCheckpointFailureInjectionSuite.scala
+++ b/sql/core/src/test/scala/org/apache/spark/sql/execution/streaming/state/RocksDBCheckpointFailureInjectionSuite.scala
@@ -70,6 +70,10 @@ class RocksDBCheckpointFailureInjectionSuite extends StreamTest
 
   implicit def toArray(str: String): Array[Byte] = if (str != null) str.getBytes else null
 
+  implicit def toStr(bytes: Array[Byte]): String = if (bytes != null) new String(bytes) else null
+
+  def toStr(kv: ByteArrayPair): (String, String) = (toStr(kv.key), toStr(kv.value))
+
   case class FailureConf(ifEnableStateStoreCheckpointIds: Boolean, fileType: String) {
     override def toString: String = {
       s"ifEnableStateStoreCheckpointIds = $ifEnableStateStoreCheckpointIds, " +
@@ -824,6 +828,62 @@ class RocksDBCheckpointFailureInjectionSuite extends StreamTest
     }
   }
 
+  /**
+   * Test that verifies that when a task is interrupted, the store's rollback() method does not
+   * throw an exception and the store can still be used after the rollback.
+   */
+  test("SPARK-54585: Interrupted task calling rollback does not throw an exception") {
+    val hadoopConf = new Configuration()
+    hadoopConf.set(
+      STREAMING_CHECKPOINT_FILE_MANAGER_CLASS.parent.key,
+      fileManagerClassName
+    )
+    withTempDirAllowFailureInjection { (remoteDir, _) =>
+      val sqlConf = new SQLConf()
+      sqlConf.setConfString("spark.sql.streaming.checkpoint.fileChecksum.enabled", "true")
+      val rocksdbChangelogCheckpointingConfKey =
+        RocksDBConf.ROCKSDB_SQL_CONF_NAME_PREFIX + ".changelogCheckpointing.enabled"
+      sqlConf.setConfString(rocksdbChangelogCheckpointingConfKey, "true")
+      val conf = RocksDBConf(StateStoreConf(sqlConf))
+
+      withDB(
+        remoteDir.getAbsolutePath,
+        version = 0,
+        conf = conf,
+        hadoopConf = hadoopConf
+      ) { db =>
+        db.put("key0", "value0")
+        val checkpointId1 = commitAndGetCheckpointId(db)
+
+        db.load(1, checkpointId1)
+        db.put("key1", "value1")
+        val checkpointId2 = commitAndGetCheckpointId(db)
+
+        db.load(2, checkpointId2)
+        db.put("key2", "value2")
+
+        // Simulate what happens when a task is killed, the thread's interrupt flag is set.
+        // This replicates the scenario where TaskContext.markTaskFailed() is called and
+        // the task failure listener invokes RocksDBStateStore.abort() -> rollback().
+        Thread.currentThread().interrupt()
+
+        // rollback() should not throw an exception
+        db.rollback()
+
+        // Clear the interrupt flag for subsequent operations
+        Thread.interrupted()
+
+        // Reload the store and insert a new value
+        db.load(2, checkpointId2)
+        db.put("key3", "value3")
+
+        // Verify the store has the correct values
+        assert(db.iterator().map(toStr).toSet ===
+          Set(("key0", "value0"), ("key1", "value1"), ("key3", "value3")))
+      }
+    }
+  }
+
   def commitAndGetCheckpointId(db: RocksDB): Option[String] = {
     val (v, ci) = db.commit()
     ci.stateStoreCkptId