diff --git a/pageserver/src/virtual_file/owned_buffers_io/io_buf_ext.rs b/pageserver/src/virtual_file/owned_buffers_io/io_buf_ext.rs
index c3940cf6ce..ede04d4957 100644
--- a/pageserver/src/virtual_file/owned_buffers_io/io_buf_ext.rs
+++ b/pageserver/src/virtual_file/owned_buffers_io/io_buf_ext.rs
@@ -27,6 +27,11 @@ where
         let FullSlice { slice: s } = self;
         s
     }
+
+    pub(crate) fn as_raw_slice(&self) -> &Slice<B> {
+        let FullSlice { slice: s } = &self;
+        s
+    }
 }
 
 impl<B> Deref for FullSlice<B>
diff --git a/pageserver/src/virtual_file/owned_buffers_io/write.rs b/pageserver/src/virtual_file/owned_buffers_io/write.rs
index c3cade5966..f383ad5723 100644
--- a/pageserver/src/virtual_file/owned_buffers_io/write.rs
+++ b/pageserver/src/virtual_file/owned_buffers_io/write.rs
@@ -1,22 +1,25 @@
 mod flush;
 use std::sync::Arc;
 
-use bytes::{BufMut, BytesMut};
+use bytes::BytesMut;
 use tokio_epoll_uring::{BoundedBufMut, IoBuf};
 
-use crate::{context::RequestContext, virtual_file::IoBufferMut};
+use crate::{
+    context::RequestContext,
+    virtual_file::{IoBuffer, IoBufferMut},
+};
 
 use super::io_buf_ext::{FullSlice, IoBufExt};
 
 /// A trait for doing owned-buffer write IO.
 /// Think [`tokio::io::AsyncWrite`] but with owned buffers.
 pub trait OwnedAsyncWriter {
-    async fn write_all_at<Buf: IoBuf + Send>(
+    fn write_all_at<Buf: IoBuf + Send>(
         &self,
         buf: FullSlice<Buf>,
         offset: u64,
         ctx: &RequestContext,
-    ) -> std::io::Result<FullSlice<Buf>>;
+    ) -> impl std::future::Future<Output = std::io::Result<FullSlice<Buf>>> + Send;
 }
 
 /// A wrapper aorund an [`OwnedAsyncWriter`] that uses a [`Buffer`] to batch
@@ -212,6 +215,8 @@ pub trait Buffer {
     fn reuse_after_flush(iobuf: Self::IoBuf) -> Self;
 }
 
+pub trait BufferMut: Buffer {}
+
 impl Buffer for BytesMut {
     type IoBuf = BytesMut;
 
@@ -240,7 +245,7 @@ impl Buffer for BytesMut {
 }
 
 impl Buffer for IoBufferMut {
-    type IoBuf = IoBufferMut;
+    type IoBuf = IoBuffer;
 
     fn cap(&self) -> usize {
         self.capacity()
@@ -256,12 +261,15 @@ impl Buffer for IoBufferMut {
     }
 
     fn flush(self) -> FullSlice<Self::IoBuf> {
-        self.slice_len()
+        self.freeze().slice_len()
     }
 
-    fn reuse_after_flush(mut iobuf: Self::IoBuf) -> Self {
-        iobuf.clear();
-        iobuf
+    fn reuse_after_flush(iobuf: Self::IoBuf) -> Self {
+        let mut recycled = iobuf
+            .into_mut()
+            .expect("buffer should only have one strong reference");
+        recycled.clear();
+        recycled
     }
 }
 
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 86cb2099e6..97b9f28009 100644
--- a/pageserver/src/virtual_file/owned_buffers_io/write/flush.rs
+++ b/pageserver/src/virtual_file/owned_buffers_io/write/flush.rs
@@ -1,19 +1,23 @@
 use std::sync::Arc;
 
 use tokio::sync::mpsc;
+use tokio_epoll_uring::IoBuf;
 
-use crate::{
-    context::RequestContext,
-    virtual_file::{IoBuffer, IoBufferMut, VirtualFile},
-};
+use crate::{context::RequestContext, virtual_file::owned_buffers_io::io_buf_ext::FullSlice};
 
-use super::{IoBufExt, OwnedAsyncWriter};
+use super::{Buffer, OwnedAsyncWriter};
 
+/// A bi-directional channel.
 pub struct Duplex<S, R> {
     pub tx: mpsc::Sender<S>,
     pub rx: mpsc::Receiver<R>,
 }
 
+/// Creates a bi-directional channel.
+///
+/// The channel will buffer up to the provided number of messages. Once the buffer is full,
+/// attempts to send new messages will wait until a message is received from the channel.
+/// The provided buffer capacity must be at least 1.
 pub fn duplex_channel<A: Send, B: Send>(buffer: usize) -> (Duplex<A, B>, Duplex<B, A>) {
     let (tx_a, rx_a) = mpsc::channel::<A>(buffer);
     let (tx_b, rx_b) = mpsc::channel::<B>(buffer);
@@ -22,95 +26,143 @@ pub fn duplex_channel<A: Send, B: Send>(buffer: usize) -> (Duplex<A, B>, Duplex<
 }
 
 impl<S: Send, R: Send> Duplex<S, R> {
+    /// Sends a value, waiting until there is capacity.
+    ///
+    /// A successful send occurs when it is determined that the other end of the channel has not hung up already.
     pub async fn send(&self, x: S) -> Result<(), mpsc::error::SendError<S>> {
         self.tx.send(x).await
     }
 
+    /// Receives the next value for this receiver.
+    ///
+    /// This method returns `None` if the channel has been closed and there are
+    /// no remaining messages in the channel's buffer.
     pub async fn recv(&mut self) -> Option<R> {
         self.rx.recv().await
     }
 }
 
-/// A handle to the flush task.
-pub struct FlushHandle {
+pub struct FlushHandleInner<Buf, W> {
     /// A bi-directional channel that sends (buffer, offset) for writes,
     /// and receives recyled buffer.
-    channel: Duplex<(IoBuffer, u64), IoBuffer>,
-    ///
-    maybe_flushed: Option<IoBuffer>,
-    join_handle: tokio::task::JoinHandle<anyhow::Result<()>>,
+    channel: Duplex<(FullSlice<Buf>, u64), FullSlice<Buf>>,
+    /// Join handle for the background flush task.
+    join_handle: tokio::task::JoinHandle<std::io::Result<Arc<W>>>,
 }
 
-pub struct FlushBackgroundTask {
-    channel: Duplex<IoBuffer, (IoBuffer, u64)>,
-    file: Arc<VirtualFile>,
+/// A handle to the flush task.
+pub struct FlushHandle<Buf, W> {
+    inner: Option<FlushHandleInner<Buf, W>>,
+    /// Buffer for serving tail reads.
+    maybe_flushed: Option<Buf>,
+}
+
+pub struct FlushBackgroundTask<Buf, W> {
+    /// A bi-directional channel that receives (buffer, offset) for writes,
+    /// and send back recycled buffer.
+    channel: Duplex<FullSlice<Buf>, (FullSlice<Buf>, u64)>,
+    writer: Arc<W>,
     ctx: RequestContext,
 }
 
-impl FlushBackgroundTask {
+impl<Buf, W> FlushBackgroundTask<Buf, W>
+where
+    Buf: IoBuf + Send + Sync,
+    W: OwnedAsyncWriter + Sync + 'static,
+{
     fn new(
-        channel: Duplex<IoBuffer, (IoBuffer, u64)>,
-        file: Arc<VirtualFile>,
+        channel: Duplex<FullSlice<Buf>, (FullSlice<Buf>, u64)>,
+        file: Arc<W>,
         ctx: RequestContext,
     ) -> Self {
-        FlushBackgroundTask { channel, file, ctx }
+        FlushBackgroundTask {
+            channel,
+            writer: file,
+            ctx,
+        }
     }
 
-    async fn run(mut self, buf: IoBufferMut) -> anyhow::Result<()> {
-        self.channel.send(buf.freeze()).await?;
+    /// Runs the background flush task.
+    async fn run(mut self, buf: FullSlice<Buf>) -> std::io::Result<Arc<W>> {
+        self.channel.send(buf).await.map_err(|_| {
+            std::io::Error::new(std::io::ErrorKind::BrokenPipe, "flush handle closed early")
+        })?;
 
-        while let Some((mut buf, offset)) = self.channel.recv().await {
-            let slice = OwnedAsyncWriter::write_all_at(
-                self.file.as_ref(),
-                buf.slice_len(),
-                offset,
-                &self.ctx,
-            )
-            .await?;
-            buf = slice.into_raw_slice().into_inner();
+        //  Exit condition: channel is closed and there is no remaining buffer to be flushed
+        while let Some((slice, offset)) = self.channel.recv().await {
+            let slice = self.writer.write_all_at(slice, offset, &self.ctx).await?;
 
-            if self.channel.send(buf).await.is_err() {
-                // Channel closed, exit task.
-                break;
+            if self.channel.send(slice).await.is_err() {
+                // Although channel is closed. Still need to finish flushing the remaining buffers.
+                continue;
             }
         }
 
-        Ok(())
+        Ok(self.writer)
     }
 }
 
-impl FlushHandle {
-    pub fn spawn_new(file: Arc<VirtualFile>, ctx: RequestContext) -> Self {
-        let (front, back) = duplex_channel(1);
+impl<Buf, W> FlushHandle<Buf, W>
+where
+    Buf: IoBuf + Send + Sync + Clone,
+    W: OwnedAsyncWriter + Send + Sync + 'static + std::fmt::Debug,
+{
+    /// Spawns a new background flush task and obtains a handle.
+    pub fn spawn_new<B>(file: Arc<W>, buf: B, ctx: RequestContext) -> Self
+    where
+        B: Buffer<IoBuf = Buf> + Send + 'static,
+    {
+        let (front, back) = duplex_channel(2);
 
         let bg = FlushBackgroundTask::new(back, file, ctx);
-        let buf = IoBufferMut::with_capacity(4096);
-        let join_handle = tokio::spawn(async move { bg.run(buf).await });
+        let join_handle = tokio::spawn(async move { bg.run(buf.flush()).await });
 
         FlushHandle {
-            channel: front,
+            inner: Some(FlushHandleInner {
+                channel: front,
+                join_handle,
+            }),
             maybe_flushed: None,
-            join_handle,
         }
     }
+
     /// Submits a buffer to be flushed in the background task.
     /// Returns a buffer that completed flushing for re-use, length reset to 0, capacity unchanged.
-    async fn flush(&mut self, buf: IoBufferMut, offset: u64) -> IoBufferMut {
-        // Send
-        let freezed = buf.freeze();
-        self.maybe_flushed.replace(freezed.clone());
-        self.channel.send((freezed, offset)).await.unwrap();
+    async fn flush<B>(&mut self, buf: B, offset: u64) -> std::io::Result<B>
+    where
+        B: Buffer<IoBuf = Buf> + Send + 'static,
+    {
+        let freezed = buf.flush();
+
+        self.maybe_flushed
+            .replace(freezed.as_raw_slice().get_ref().clone());
+
+        let submit = self.inner_mut().channel.send((freezed, offset)).await;
+
+        if submit.is_err() {
+            return self.handle_error().await;
+        }
 
         // Wait for an available buffer from the background flush task.
-        let recycled = self.channel.recv().await.unwrap();
+        let Some(recycled) = self.inner_mut().channel.recv().await else {
+            return self.handle_error().await;
+        };
 
         // The only other place that could hold a reference to the recycled buffer
         // is in `Self::maybe_flushed`, but we have already replace it with the new buffer.
-        let mut recycled = recycled
-            .into_mut()
-            .expect("buffer should only have one strong reference");
+        Ok(Buffer::reuse_after_flush(
+            recycled.into_raw_slice().into_inner(),
+        ))
+    }
 
-        recycled.clear();
-        recycled
+    fn inner_mut(&mut self) -> &mut FlushHandleInner<Buf, W> {
+        self.inner.as_mut().unwrap()
+    }
+
+    async fn handle_error<T>(&mut self) -> std::io::Result<T> {
+        let handle = self.inner.take().unwrap();
+        drop(handle.channel.tx);
+        let e = handle.join_handle.await.unwrap().unwrap_err();
+        return Err(e);
     }
 }