diff --git a/cli/tests/unit/kv_test.ts b/cli/tests/unit/kv_test.ts
index da5dba6af2..25abf4cde2 100644
--- a/cli/tests/unit/kv_test.ts
+++ b/cli/tests/unit/kv_test.ts
@@ -1819,6 +1819,16 @@ Deno.test({
   },
 });
 
+Deno.test({
+  name: "queue graceful close",
+  async fn() {
+    const db: Deno.Kv = await Deno.openKv(":memory:");
+    const listener = db.listenQueue((_msg) => {});
+    db.close();
+    await listener;
+  },
+});
+
 dbTest("atomic operation is exposed", (db) => {
   assert(Deno.AtomicOperation);
   const ao = db.atomic();
diff --git a/ext/kv/01_db.ts b/ext/kv/01_db.ts
index e934a3b6dc..6e8a571f0c 100644
--- a/ext/kv/01_db.ts
+++ b/ext/kv/01_db.ts
@@ -61,7 +61,6 @@ const kvSymbol = Symbol("KvRid");
 
 class Kv {
   #rid: number;
-  #closed: boolean;
 
   constructor(rid: number = undefined, symbol: symbol = undefined) {
     if (kvSymbol !== symbol) {
@@ -70,7 +69,6 @@ class Kv {
       );
     }
     this.#rid = rid;
-    this.#closed = false;
   }
 
   atomic() {
@@ -251,20 +249,14 @@ class Kv {
     handler: (message: unknown) => Promise<void> | void,
   ): Promise<void> {
     const finishMessageOps = new Map<number, Promise<void>>();
-    while (!this.#closed) {
+    while (true) {
       // Wait for the next message.
-      let next: { 0: Uint8Array; 1: number };
-      try {
-        next = await core.opAsync(
-          "op_kv_dequeue_next_message",
-          this.#rid,
-        );
-      } catch (error) {
-        if (this.#closed) {
-          break;
-        } else {
-          throw error;
-        }
+      const next: { 0: Uint8Array; 1: number } = await core.opAsync(
+        "op_kv_dequeue_next_message",
+        this.#rid,
+      );
+      if (next === null) {
+        break;
       }
 
       // Deserialize the payload.
@@ -283,20 +275,16 @@ class Kv {
         } catch (error) {
           console.error("Exception in queue handler", error);
         } finally {
-          if (this.#closed) {
-            core.close(handleId);
-          } else {
-            const promise: Promise<void> = core.opAsync(
-              "op_kv_finish_dequeued_message",
-              handleId,
-              success,
-            );
-            finishMessageOps.set(handleId, promise);
-            try {
-              await promise;
-            } finally {
-              finishMessageOps.delete(handleId);
-            }
+          const promise: Promise<void> = core.opAsync(
+            "op_kv_finish_dequeued_message",
+            handleId,
+            success,
+          );
+          finishMessageOps.set(handleId, promise);
+          try {
+            await promise;
+          } finally {
+            finishMessageOps.delete(handleId);
           }
         }
       })();
@@ -310,7 +298,6 @@ class Kv {
 
   close() {
     core.close(this.#rid);
-    this.#closed = true;
   }
 }
 
diff --git a/ext/kv/dynamic.rs b/ext/kv/dynamic.rs
index f79c10f559..9084cc1bf2 100644
--- a/ext/kv/dynamic.rs
+++ b/ext/kv/dynamic.rs
@@ -132,7 +132,7 @@ pub trait DynamicDb {
   async fn dyn_dequeue_next_message(
     &self,
     state: Rc<RefCell<OpState>>,
-  ) -> Result<Box<dyn QueueMessageHandle>, AnyError>;
+  ) -> Result<Option<Box<dyn QueueMessageHandle>>, AnyError>;
 
   fn dyn_close(&self);
 }
@@ -161,7 +161,7 @@ impl Database for Box<dyn DynamicDb> {
   async fn dequeue_next_message(
     &self,
     state: Rc<RefCell<OpState>>,
-  ) -> Result<Box<dyn QueueMessageHandle>, AnyError> {
+  ) -> Result<Option<Box<dyn QueueMessageHandle>>, AnyError> {
     (**self).dyn_dequeue_next_message(state).await
   }
 
@@ -196,8 +196,13 @@ where
   async fn dyn_dequeue_next_message(
     &self,
     state: Rc<RefCell<OpState>>,
-  ) -> Result<Box<dyn QueueMessageHandle>, AnyError> {
-    Ok(Box::new(self.dequeue_next_message(state).await?))
+  ) -> Result<Option<Box<dyn QueueMessageHandle>>, AnyError> {
+    Ok(
+      self
+        .dequeue_next_message(state)
+        .await?
+        .map(|x| Box::new(x) as Box<dyn QueueMessageHandle>),
+    )
   }
 
   fn dyn_close(&self) {
diff --git a/ext/kv/interface.rs b/ext/kv/interface.rs
index abeaf8dd51..1acf3ce165 100644
--- a/ext/kv/interface.rs
+++ b/ext/kv/interface.rs
@@ -43,7 +43,7 @@ pub trait Database {
   async fn dequeue_next_message(
     &self,
     state: Rc<RefCell<OpState>>,
-  ) -> Result<Self::QMH, AnyError>;
+  ) -> Result<Option<Self::QMH>, AnyError>;
 
   fn close(&self);
 }
diff --git a/ext/kv/lib.rs b/ext/kv/lib.rs
index 72d5e862b0..762009d2a4 100644
--- a/ext/kv/lib.rs
+++ b/ext/kv/lib.rs
@@ -16,6 +16,7 @@ use chrono::Utc;
 use codec::decode_key;
 use codec::encode_key;
 use deno_core::anyhow::Context;
+use deno_core::error::get_custom_error_class;
 use deno_core::error::type_error;
 use deno_core::error::AnyError;
 use deno_core::op2;
@@ -322,24 +323,35 @@ impl<QMH: QueueMessageHandle + 'static> Resource for QueueMessageResource<QMH> {
 async fn op_kv_dequeue_next_message<DBH>(
   state: Rc<RefCell<OpState>>,
   #[smi] rid: ResourceId,
-) -> Result<(ToJsBuffer, ResourceId), AnyError>
+) -> Result<Option<(ToJsBuffer, ResourceId)>, AnyError>
 where
   DBH: DatabaseHandler + 'static,
 {
   let db = {
     let state = state.borrow();
     let resource =
-      state.resource_table.get::<DatabaseResource<DBH::DB>>(rid)?;
+      match state.resource_table.get::<DatabaseResource<DBH::DB>>(rid) {
+        Ok(resource) => resource,
+        Err(err) => {
+          if get_custom_error_class(&err) == Some("BadResource") {
+            return Ok(None);
+          } else {
+            return Err(err);
+          }
+        }
+      };
     resource.db.clone()
   };
 
-  let mut handle = db.dequeue_next_message(state.clone()).await?;
+  let Some(mut handle) = db.dequeue_next_message(state.clone()).await? else {
+    return Ok(None);
+  };
   let payload = handle.take_payload().await?.into();
   let handle_rid = {
     let mut state = state.borrow_mut();
     state.resource_table.add(QueueMessageResource { handle })
   };
-  Ok((payload, handle_rid))
+  Ok(Some((payload, handle_rid)))
 }
 
 #[op2(async)]
diff --git a/ext/kv/remote.rs b/ext/kv/remote.rs
index fc18e4615d..36c4d3af20 100644
--- a/ext/kv/remote.rs
+++ b/ext/kv/remote.rs
@@ -277,7 +277,7 @@ impl<P: RemoteDbHandlerPermissions> Database for RemoteDb<P> {
   async fn dequeue_next_message(
     &self,
     _state: Rc<RefCell<OpState>>,
-  ) -> Result<Self::QMH, AnyError> {
+  ) -> Result<Option<Self::QMH>, AnyError> {
     let msg = "Deno.Kv.listenQueue is not supported for remote KV databases";
     eprintln!("{}", yellow(msg));
     deno_core::futures::future::pending().await
diff --git a/ext/kv/sqlite.rs b/ext/kv/sqlite.rs
index ceeb98c259..192141e275 100644
--- a/ext/kv/sqlite.rs
+++ b/ext/kv/sqlite.rs
@@ -395,9 +395,7 @@ impl QueueMessageHandle for DequeuedMessage {
       Err(e) => {
         // Silently ignore the error if the database has been closed
         // This message will be delivered on the next run
-        if get_custom_error_class(&e) == Some("TypeError")
-          && e.to_string() == ERROR_USING_CLOSED_DATABASE
-        {
+        if is_conn_closed_error(&e) {
           return Ok(());
         }
         return Err(e);
@@ -437,25 +435,25 @@ impl SqliteQueue {
 
     spawn(async move {
       // Oneshot requeue of all inflight messages.
-      Self::requeue_inflight_messages(conn.clone()).await.unwrap();
+      if let Err(e) = Self::requeue_inflight_messages(conn.clone()).await {
+        // Exit the dequeue loop cleanly if the database has been closed.
+        if is_conn_closed_error(&e) {
+          return;
+        }
+        panic!("kv: Error in requeue_inflight_messages: {}", e);
+      }
 
       // Continuous dequeue loop.
-      match Self::dequeue_loop(conn.clone(), dequeue_tx, shutdown_rx, waker_rx)
-        .await
+      if let Err(e) =
+        Self::dequeue_loop(conn.clone(), dequeue_tx, shutdown_rx, waker_rx)
+          .await
       {
-        Ok(_) => Ok(()),
-        Err(e) => {
-          // Exit the dequeue loop cleanly if the database has been closed.
-          if get_custom_error_class(&e) == Some("TypeError")
-            && e.to_string() == ERROR_USING_CLOSED_DATABASE
-          {
-            Ok(())
-          } else {
-            Err(e)
-          }
+        // Exit the dequeue loop cleanly if the database has been closed.
+        if is_conn_closed_error(&e) {
+          return;
         }
+        panic!("kv: Error in dequeue_loop: {}", e);
       }
-      .unwrap();
     });
 
     Self {
@@ -467,25 +465,25 @@ impl SqliteQueue {
     }
   }
 
-  async fn dequeue(&self) -> Result<DequeuedMessage, AnyError> {
+  async fn dequeue(&self) -> Result<Option<DequeuedMessage>, AnyError> {
     // Wait for the next message to be available from dequeue_rx.
     let (payload, id) = {
       let mut queue_rx = self.dequeue_rx.borrow_mut().await;
       let Some(msg) = queue_rx.recv().await else {
-        return Err(type_error("Database closed"));
+        return Ok(None);
       };
       msg
     };
 
     let permit = self.concurrency_limiter.clone().acquire_owned().await?;
 
-    Ok(DequeuedMessage {
+    Ok(Some(DequeuedMessage {
       conn: self.conn.downgrade(),
       id,
       payload: Some(payload),
       waker_tx: self.waker_tx.clone(),
       _permit: permit,
-    })
+    }))
   }
 
   async fn wake(&self) -> Result<(), AnyError> {
@@ -904,7 +902,7 @@ impl Database for SqliteDb {
   async fn dequeue_next_message(
     &self,
     _state: Rc<RefCell<OpState>>,
-  ) -> Result<Self::QMH, AnyError> {
+  ) -> Result<Option<Self::QMH>, AnyError> {
     let queue = self
       .queue
       .get_or_init(|| async move { SqliteQueue::new(self.conn.clone()) })
@@ -1013,3 +1011,8 @@ fn encode_value(value: &crate::Value) -> (Cow<'_, [u8]>, i64) {
     }
   }
 }
+
+fn is_conn_closed_error(e: &AnyError) -> bool {
+  get_custom_error_class(e) == Some("TypeError")
+    && e.to_string() == ERROR_USING_CLOSED_DATABASE
+}