diff --git a/pageserver/benches/bench_ingest.rs b/pageserver/benches/bench_ingest.rs
index caacd365b306..b67a9cc47951 100644
--- a/pageserver/benches/bench_ingest.rs
+++ b/pageserver/benches/bench_ingest.rs
@@ -62,10 +62,8 @@ async fn ingest(
     let ctx = RequestContext::new(TaskKind::DebugTool, DownloadBehavior::Error);
 
     let gate = utils::sync::gate::Gate::default();
-    let entered = gate.enter().unwrap();
 
-    let layer =
-        InMemoryLayer::create(conf, timeline_id, tenant_shard_id, lsn, entered, &ctx).await?;
+    let layer = InMemoryLayer::create(conf, timeline_id, tenant_shard_id, lsn, &gate, &ctx).await?;
 
     let data = Value::Image(Bytes::from(vec![0u8; put_size]));
     let data_ser_size = data.serialized_size().unwrap() as usize;
diff --git a/pageserver/src/tenant/ephemeral_file.rs b/pageserver/src/tenant/ephemeral_file.rs
index 9aecfff384eb..aaec8a4c313a 100644
--- a/pageserver/src/tenant/ephemeral_file.rs
+++ b/pageserver/src/tenant/ephemeral_file.rs
@@ -38,9 +38,9 @@ impl EphemeralFile {
         conf: &PageServerConf,
         tenant_shard_id: TenantShardId,
         timeline_id: TimelineId,
-        gate_guard: utils::sync::gate::GateGuard,
+        gate: &utils::sync::gate::Gate,
         ctx: &RequestContext,
-    ) -> Result<EphemeralFile, io::Error> {
+    ) -> anyhow::Result<EphemeralFile> {
         static NEXT_FILENAME: AtomicU64 = AtomicU64::new(1);
         let filename_disambiguator =
             NEXT_FILENAME.fetch_add(1, std::sync::atomic::Ordering::Relaxed);
@@ -73,9 +73,10 @@ impl EphemeralFile {
             buffered_writer: owned_buffers_io::write::BufferedWriter::new(
                 file,
                 || IoBufferMut::with_capacity(TAIL_SZ),
+                gate.enter()?,
                 ctx,
             ),
-            _gate_guard: gate_guard,
+            _gate_guard: gate.enter()?,
         })
     }
 }
@@ -362,7 +363,7 @@ mod tests {
 
         let gate = utils::sync::gate::Gate::default();
 
-        let file = EphemeralFile::create(conf, tenant_id, timeline_id, gate.enter().unwrap(), &ctx)
+        let file = EphemeralFile::create(conf, tenant_id, timeline_id, &gate, &ctx)
             .await
             .unwrap();
 
@@ -393,10 +394,9 @@ mod tests {
 
         let gate = utils::sync::gate::Gate::default();
 
-        let mut file =
-            EphemeralFile::create(conf, tenant_id, timeline_id, gate.enter().unwrap(), &ctx)
-                .await
-                .unwrap();
+        let mut file = EphemeralFile::create(conf, tenant_id, timeline_id, &gate, &ctx)
+            .await
+            .unwrap();
 
         let mutable = file.buffered_writer.inspect_mutable();
         let cap = mutable.capacity();
@@ -451,10 +451,9 @@ mod tests {
 
         let gate = utils::sync::gate::Gate::default();
 
-        let mut file =
-            EphemeralFile::create(conf, tenant_id, timeline_id, gate.enter().unwrap(), &ctx)
-                .await
-                .unwrap();
+        let mut file = EphemeralFile::create(conf, tenant_id, timeline_id, &gate, &ctx)
+            .await
+            .unwrap();
 
         // mutable buffer and maybe_flushed buffer each has `cap` bytes.
         let cap = file.buffered_writer.inspect_mutable().capacity();
@@ -499,10 +498,9 @@ mod tests {
 
         let gate = utils::sync::gate::Gate::default();
 
-        let mut file =
-            EphemeralFile::create(conf, tenant_id, timeline_id, gate.enter().unwrap(), &ctx)
-                .await
-                .unwrap();
+        let mut file = EphemeralFile::create(conf, tenant_id, timeline_id, &gate, &ctx)
+            .await
+            .unwrap();
 
         let mutable = file.buffered_writer.inspect_mutable();
         let cap = mutable.capacity();
diff --git a/pageserver/src/tenant/remote_timeline_client.rs b/pageserver/src/tenant/remote_timeline_client.rs
index 007bd3eef083..2982cfb16c3e 100644
--- a/pageserver/src/tenant/remote_timeline_client.rs
+++ b/pageserver/src/tenant/remote_timeline_client.rs
@@ -681,6 +681,7 @@ impl RemoteTimelineClient {
         layer_file_name: &LayerName,
         layer_metadata: &LayerFileMetadata,
         local_path: &Utf8Path,
+        gate: &utils::sync::gate::Gate,
         cancel: &CancellationToken,
         ctx: &RequestContext,
     ) -> Result<u64, DownloadError> {
@@ -700,6 +701,7 @@ impl RemoteTimelineClient {
                 layer_file_name,
                 layer_metadata,
                 local_path,
+                gate,
                 cancel,
                 ctx,
             )
diff --git a/pageserver/src/tenant/remote_timeline_client/download.rs b/pageserver/src/tenant/remote_timeline_client/download.rs
index 41e32a1aa3ba..4f7a51ee68f1 100644
--- a/pageserver/src/tenant/remote_timeline_client/download.rs
+++ b/pageserver/src/tenant/remote_timeline_client/download.rs
@@ -57,6 +57,7 @@ pub async fn download_layer_file<'a>(
     layer_file_name: &'a LayerName,
     layer_metadata: &'a LayerFileMetadata,
     local_path: &Utf8Path,
+    gate: &utils::sync::gate::Gate,
     cancel: &CancellationToken,
     ctx: &RequestContext,
 ) -> Result<u64, DownloadError> {
@@ -85,7 +86,9 @@ pub async fn download_layer_file<'a>(
     let temp_file_path = path_with_suffix_extension(local_path, TEMP_DOWNLOAD_EXTENSION);
 
     let bytes_amount = download_retry(
-        || async { download_object(storage, &remote_path, &temp_file_path, cancel, ctx).await },
+        || async {
+            download_object(storage, &remote_path, &temp_file_path, gate, cancel, ctx).await
+        },
         &format!("download {remote_path:?}"),
         cancel,
     )
@@ -145,6 +148,7 @@ async fn download_object<'a>(
     storage: &'a GenericRemoteStorage,
     src_path: &RemotePath,
     dst_path: &Utf8PathBuf,
+    gate: &utils::sync::gate::Gate,
     cancel: &CancellationToken,
     #[cfg_attr(target_os = "macos", allow(unused_variables))] ctx: &RequestContext,
 ) -> Result<u64, DownloadError> {
@@ -219,15 +223,16 @@ async fn download_object<'a>(
 
                 pausable_failpoint!("before-downloading-layer-stream-pausable");
 
+                let mut buffered = owned_buffers_io::write::BufferedWriter::<IoBufferMut, _>::new(
+                    destination_file,
+                    || IoBufferMut::with_capacity(super::BUFFER_SIZE),
+                    gate.enter().map_err(|_| DownloadError::Cancelled)?,
+                    ctx,
+                );
+
                 // TODO: use vectored write (writev) once supported by tokio-epoll-uring.
                 // There's chunks_vectored() on the stream.
                 let (bytes_amount, destination_file) = async {
-                    let mut buffered =
-                        owned_buffers_io::write::BufferedWriter::<IoBufferMut, _>::new(
-                            destination_file,
-                            || IoBufferMut::with_capacity(super::BUFFER_SIZE),
-                            ctx,
-                        );
                     while let Some(res) =
                         futures::StreamExt::next(&mut download.download_stream).await
                     {
diff --git a/pageserver/src/tenant/secondary/downloader.rs b/pageserver/src/tenant/secondary/downloader.rs
index 7443261a9c00..03d40cffe3c3 100644
--- a/pageserver/src/tenant/secondary/downloader.rs
+++ b/pageserver/src/tenant/secondary/downloader.rs
@@ -1181,6 +1181,7 @@ impl<'a> TenantDownloader<'a> {
             &layer.name,
             &layer.metadata,
             &local_path,
+            &self.secondary_state.gate,
             &self.secondary_state.cancel,
             ctx,
         )
diff --git a/pageserver/src/tenant/storage_layer/inmemory_layer.rs b/pageserver/src/tenant/storage_layer/inmemory_layer.rs
index af6112d53550..71e53da20f7f 100644
--- a/pageserver/src/tenant/storage_layer/inmemory_layer.rs
+++ b/pageserver/src/tenant/storage_layer/inmemory_layer.rs
@@ -555,13 +555,12 @@ impl InMemoryLayer {
         timeline_id: TimelineId,
         tenant_shard_id: TenantShardId,
         start_lsn: Lsn,
-        gate_guard: utils::sync::gate::GateGuard,
+        gate: &utils::sync::gate::Gate,
         ctx: &RequestContext,
     ) -> Result<InMemoryLayer> {
         trace!("initializing new empty InMemoryLayer for writing on timeline {timeline_id} at {start_lsn}");
 
-        let file =
-            EphemeralFile::create(conf, tenant_shard_id, timeline_id, gate_guard, ctx).await?;
+        let file = EphemeralFile::create(conf, tenant_shard_id, timeline_id, gate, ctx).await?;
         let key = InMemoryLayerFileId(file.page_cache_file_id());
 
         Ok(InMemoryLayer {
diff --git a/pageserver/src/tenant/storage_layer/layer.rs b/pageserver/src/tenant/storage_layer/layer.rs
index a9f1189b4112..8933e8ceb13e 100644
--- a/pageserver/src/tenant/storage_layer/layer.rs
+++ b/pageserver/src/tenant/storage_layer/layer.rs
@@ -1149,6 +1149,7 @@ impl LayerInner {
                 &self.desc.layer_name(),
                 &self.metadata(),
                 &self.path,
+                &timeline.gate,
                 &timeline.cancel,
                 ctx,
             )
diff --git a/pageserver/src/tenant/timeline.rs b/pageserver/src/tenant/timeline.rs
index f6a06e73a790..347393ba5654 100644
--- a/pageserver/src/tenant/timeline.rs
+++ b/pageserver/src/tenant/timeline.rs
@@ -3471,7 +3471,6 @@ impl Timeline {
         ctx: &RequestContext,
     ) -> anyhow::Result<Arc<InMemoryLayer>> {
         let mut guard = self.layers.write().await;
-        let gate_guard = self.gate.enter().context("enter gate for inmem layer")?;
 
         let last_record_lsn = self.get_last_record_lsn();
         ensure!(
@@ -3488,7 +3487,7 @@ impl Timeline {
                 self.conf,
                 self.timeline_id,
                 self.tenant_shard_id,
-                gate_guard,
+                &self.gate,
                 ctx,
             )
             .await?;
diff --git a/pageserver/src/tenant/timeline/layer_manager.rs b/pageserver/src/tenant/timeline/layer_manager.rs
index 4293a44dca25..88baa88f24b8 100644
--- a/pageserver/src/tenant/timeline/layer_manager.rs
+++ b/pageserver/src/tenant/timeline/layer_manager.rs
@@ -182,7 +182,7 @@ impl OpenLayerManager {
         conf: &'static PageServerConf,
         timeline_id: TimelineId,
         tenant_shard_id: TenantShardId,
-        gate_guard: utils::sync::gate::GateGuard,
+        gate: &utils::sync::gate::Gate,
         ctx: &RequestContext,
     ) -> anyhow::Result<Arc<InMemoryLayer>> {
         ensure!(lsn.is_aligned());
@@ -212,15 +212,9 @@ impl OpenLayerManager {
                 lsn
             );
 
-            let new_layer = InMemoryLayer::create(
-                conf,
-                timeline_id,
-                tenant_shard_id,
-                start_lsn,
-                gate_guard,
-                ctx,
-            )
-            .await?;
+            let new_layer =
+                InMemoryLayer::create(conf, timeline_id, tenant_shard_id, start_lsn, &gate, ctx)
+                    .await?;
             let layer = Arc::new(new_layer);
 
             self.layer_map.open_layer = Some(layer.clone());
diff --git a/pageserver/src/virtual_file/owned_buffers_io/write.rs b/pageserver/src/virtual_file/owned_buffers_io/write.rs
index d2e85bda2bf3..9edb2141e9f4 100644
--- a/pageserver/src/virtual_file/owned_buffers_io/write.rs
+++ b/pageserver/src/virtual_file/owned_buffers_io/write.rs
@@ -68,11 +68,21 @@ where
     /// Creates a new buffered writer.
     ///
     /// The `buf_new` function provides a way to initialize the owned buffers used by this writer.
-    pub fn new(writer: Arc<W>, buf_new: impl Fn() -> B, ctx: &RequestContext) -> Self {
+    pub fn new(
+        writer: Arc<W>,
+        buf_new: impl Fn() -> B,
+        gate_guard: utils::sync::gate::GateGuard,
+        ctx: &RequestContext,
+    ) -> Self {
         Self {
             writer: writer.clone(),
             mutable: Some(buf_new()),
-            flush_handle: FlushHandle::spawn_new(writer, buf_new(), ctx.attached_child()),
+            flush_handle: FlushHandle::spawn_new(
+                writer,
+                buf_new(),
+                gate_guard,
+                ctx.attached_child(),
+            ),
             bytes_submitted: 0,
         }
     }
@@ -302,13 +312,15 @@ mod tests {
     }
 
     #[tokio::test]
-    async fn test_write_all_borrowed_always_goes_through_buffer() -> std::io::Result<()> {
+    async fn test_write_all_borrowed_always_goes_through_buffer() -> anyhow::Result<()> {
         let ctx = test_ctx();
         let ctx = &ctx;
         let recorder = Arc::new(RecorderWriter::default());
+        let gate = utils::sync::gate::Gate::default();
         let mut writer = BufferedWriter::<_, RecorderWriter>::new(
             recorder,
             || IoBufferMut::with_capacity(2),
+            gate.enter()?,
             ctx,
         );
 
diff --git a/pageserver/src/virtual_file/owned_buffers_io/write/flush.rs b/pageserver/src/virtual_file/owned_buffers_io/write/flush.rs
index 9ec49c33a890..5b3997963ead 100644
--- a/pageserver/src/virtual_file/owned_buffers_io/write/flush.rs
+++ b/pageserver/src/virtual_file/owned_buffers_io/write/flush.rs
@@ -115,14 +115,19 @@ where
     /// Spawns a new background flush task and obtains a handle.
     ///
     /// Note: The background task so we do not need to explicitly maintain a queue of buffers.
-    pub fn spawn_new<B>(file: Arc<W>, buf: B, ctx: RequestContext) -> Self
+    pub fn spawn_new<B>(
+        file: Arc<W>,
+        buf: B,
+        gate_guard: utils::sync::gate::GateGuard,
+        ctx: RequestContext,
+    ) -> Self
     where
         B: Buffer<IoBuf = Buf> + Send + 'static,
     {
         let (front, back) = duplex::mpsc::channel(2);
 
         let join_handle = tokio::spawn(async move {
-            FlushBackgroundTask::new(back, file, ctx)
+            FlushBackgroundTask::new(back, file, gate_guard, ctx)
                 .run(buf.flush())
                 .await
         });
@@ -200,6 +205,8 @@ pub struct FlushBackgroundTask<Buf, W> {
     /// A writter for persisting data to disk.
     writer: Arc<W>,
     ctx: RequestContext,
+    /// Prevent timeline from shuting down until the flush background task finishes flushing all remaining buffers to disk.
+    _gate_guard: utils::sync::gate::GateGuard,
 }
 
 impl<Buf, W> FlushBackgroundTask<Buf, W>
@@ -211,11 +218,13 @@ where
     fn new(
         channel: duplex::mpsc::Duplex<FullSlice<Buf>, FlushRequest<Buf>>,
         file: Arc<W>,
+        gate_guard: utils::sync::gate::GateGuard,
         ctx: RequestContext,
     ) -> Self {
         FlushBackgroundTask {
             channel,
             writer: file,
+            _gate_guard: gate_guard,
             ctx,
         }
     }