diff --git a/pageserver/src/page_service.rs b/pageserver/src/page_service.rs
index bbd2d0e76e..1013131a99 100644
--- a/pageserver/src/page_service.rs
+++ b/pageserver/src/page_service.rs
@@ -384,11 +384,17 @@ impl PageServerHandler {
         }
     }
 
-    /// Analogous to calling cancelled() on a Timeline's cancellation token: waits for cancellation.
+    /// Future that completes when we need to shut down the connection.
     ///
-    /// We use many Timeline objects, and hold GateGuards on all of them.  We must therefore respect
-    /// all of their cancellation tokens.
-    async fn timeline_cancelled(&self) {
+    /// Reasons for need to shut down are:
+    /// - any of the timelines we hold GateGuards for in `shard_timelines` is cancelled
+    /// - task_mgr requests shutdown of the connection
+    ///
+    /// The need to check for `task_mgr` cancellation arises mainly from `handle_pagerequests`
+    /// where, at first, `shard_timelines` is empty, see <https://github.com/neondatabase/neon/pull/6388>
+    ///
+    /// NB: keep in sync with [`Self::is_connection_cancelled`]
+    async fn await_connection_cancelled(&self) {
         // A short wait before we expend the cycles to walk our timeline map.  This avoids incurring
         // that cost every time we check for cancellation.
         tokio::time::sleep(Duration::from_millis(10)).await;
@@ -404,14 +410,19 @@ impl PageServerHandler {
             .map(|ht| ht.timeline.cancel.cancelled())
             .collect::<FuturesUnordered<_>>();
 
-        futs.next().await;
+        tokio::select! {
+            _ = task_mgr::shutdown_watcher() => { }
+            _ = futs.next() => {}
+        }
     }
 
-    /// Analogous to calling is_cancelled() on a Timeline's cancellation token
-    fn timeline_is_cancelled(&self) -> bool {
-        self.shard_timelines
-            .values()
-            .any(|ht| ht.timeline.cancel.is_cancelled() || ht.timeline.is_stopping())
+    /// Checking variant of [`Self::await_connection_cancelled`].
+    fn is_connection_cancelled(&self) -> bool {
+        task_mgr::is_shutdown_requested()
+            || self
+                .shard_timelines
+                .values()
+                .any(|ht| ht.timeline.cancel.is_cancelled() || ht.timeline.is_stopping())
     }
 
     /// This function always respects cancellation of any timeline in `[Self::shard_timelines]`.  Pass in
@@ -432,7 +443,7 @@ impl PageServerHandler {
             flush_r = pgb.flush() => {
                 Ok(flush_r?)
             },
-            _ = self.timeline_cancelled() => {
+            _ = self.await_connection_cancelled() => {
                 Err(QueryError::Shutdown)
             }
             _ = cancel.cancelled() => {
@@ -549,7 +560,7 @@ impl PageServerHandler {
             let msg = tokio::select! {
                 biased;
 
-                _ = self.timeline_cancelled() => {
+                _ = self.await_connection_cancelled() => {
                     // We were requested to shut down.
                     info!("shutdown request received in page handler");
                     return Err(QueryError::Shutdown)
@@ -632,7 +643,7 @@ impl PageServerHandler {
                     span.in_scope(|| info!("handler requested reconnect: {reason}"));
                     return Err(QueryError::Reconnect);
                 }
-                Err(e) if self.timeline_is_cancelled() => {
+                Err(e) if self.is_connection_cancelled() => {
                     // This branch accomodates code within request handlers that returns an anyhow::Error instead of a clean
                     // shutdown error, this may be buried inside a PageReconstructError::Other for example.
                     //