diff --git a/Cargo.lock b/Cargo.lock
index c6c1f4df2b6a..28d0778c05eb 100644
--- a/Cargo.lock
+++ b/Cargo.lock
@@ -5158,7 +5158,7 @@ dependencies = [
 [[package]]
 name = "tokio-epoll-uring"
 version = "0.1.0"
-source = "git+https://github.com/neondatabase/tokio-epoll-uring.git?branch=main#53c832d322244f704c7612125496df5ac117ac39"
+source = "git+https://github.com/neondatabase/tokio-epoll-uring.git?branch=problame/generic-owned-fd#c57c5867ae9511f2f2d9ba170f493bbab73a2eee"
 dependencies = [
  "futures",
  "once_cell",
@@ -5714,7 +5714,7 @@ dependencies = [
 [[package]]
 name = "uring-common"
 version = "0.1.0"
-source = "git+https://github.com/neondatabase/tokio-epoll-uring.git?branch=main#53c832d322244f704c7612125496df5ac117ac39"
+source = "git+https://github.com/neondatabase/tokio-epoll-uring.git?branch=problame/generic-owned-fd#c57c5867ae9511f2f2d9ba170f493bbab73a2eee"
 dependencies = [
  "io-uring",
  "libc",
diff --git a/pageserver/Cargo.toml b/pageserver/Cargo.toml
index 76dc6a576458..ab8e192d17da 100644
--- a/pageserver/Cargo.toml
+++ b/pageserver/Cargo.toml
@@ -85,7 +85,7 @@ strum.workspace = true
 strum_macros.workspace = true
 # WIP PR: https://github.com/neondatabase/tokio-epoll-uring/pull/25
 #tokio-epoll-uring = { path = "../../tokio-epoll-uring/tokio-epoll-uring" }
-tokio-epoll-uring = { git = "https://github.com/neondatabase/tokio-epoll-uring.git" , branch = "main" }
+tokio-epoll-uring = { git = "https://github.com/neondatabase/tokio-epoll-uring.git" , branch = "problame/generic-owned-fd" }
 
 [dev-dependencies]
 criterion.workspace = true
diff --git a/pageserver/src/virtual_file.rs b/pageserver/src/virtual_file.rs
index 5042aa50612e..f7782c1c8b24 100644
--- a/pageserver/src/virtual_file.rs
+++ b/pageserver/src/virtual_file.rs
@@ -16,9 +16,10 @@ use camino::{Utf8Path, Utf8PathBuf};
 use once_cell::sync::OnceCell;
 use std::fs::{self, File};
 use std::io::{Error, ErrorKind, Seek, SeekFrom};
-use std::os::fd::{AsRawFd, FromRawFd, IntoRawFd, OwnedFd};
+use std::os::fd::{AsFd, AsRawFd, BorrowedFd, FromRawFd, IntoRawFd, OwnedFd, RawFd};
 use std::os::unix::fs::FileExt;
 use std::sync::atomic::{AtomicBool, AtomicUsize, Ordering};
+use std::sync::Arc;
 use tokio::sync::{RwLock, RwLockReadGuard, RwLockWriteGuard};
 use tokio::time::Instant;
 use utils::fs_ext;
@@ -105,7 +106,7 @@ struct SlotInner {
     tag: u64,
 
     /// the underlying file
-    file: Option<File>,
+    file: Option<OwnedFd>,
 }
 
 impl OpenFiles {
@@ -270,7 +271,7 @@ macro_rules! observe_duration {
 
 macro_rules! with_file {
     ($this:expr, $op:expr, | $ident:ident | $($body:tt)*) => {{
-        let $ident = $this.lock_file().await?;
+        let mut $ident = $this.lock_file().await?;
         observe_duration!($op, $($body)*)
     }};
 }
@@ -424,7 +425,6 @@ impl VirtualFile {
                         std::io::Error::new(std::io::ErrorKind::Other, system)
                     }
                 })?;
-            let file = File::from(file);
             file
         }));
 
@@ -452,15 +452,13 @@ impl VirtualFile {
 
     /// Call File::sync_all() on the underlying File.
     pub async fn sync_all(&self) -> Result<(), Error> {
-        with_file!(self, StorageIoOperation::Fsync, |file| file
-            .as_ref()
-            .sync_all())
+        with_file!(self, StorageIoOperation::Fsync, |file_guard| file_guard
+            .with_std_file(|std_file| std_file.sync_all()))
     }
 
     pub async fn metadata(&self) -> Result<fs::Metadata, Error> {
-        with_file!(self, StorageIoOperation::Metadata, |file| file
-            .as_ref()
-            .metadata())
+        with_file!(self, StorageIoOperation::Metadata, |file_guard| file_guard
+            .with_std_file(|std_file| std_file.metadata()))
     }
 
     /// Helper function internal to `VirtualFile` that looks up the underlying File,
@@ -526,7 +524,6 @@ impl VirtualFile {
                         std::io::Error::new(std::io::ErrorKind::Other, system)
                     }
                 })?;
-            let file = File::from(file);
             file
         });
 
@@ -553,9 +550,8 @@ impl VirtualFile {
                 self.pos = offset;
             }
             SeekFrom::End(offset) => {
-                self.pos = with_file!(self, StorageIoOperation::Seek, |file| file
-                    .as_ref()
-                    .seek(SeekFrom::End(offset)))?
+                self.pos = with_file!(self, StorageIoOperation::Seek, |file_guard| file_guard
+                    .with_std_file(|std_file| std_file.seek(SeekFrom::End(offset))))?
             }
             SeekFrom::Current(offset) => {
                 let pos = self.pos as i128 + offset as i128;
@@ -620,13 +616,7 @@ impl VirtualFile {
             buf: write_guard,
             init_up_to: 0,
         };
-        let owned_fd = unsafe { OwnedFd::from_raw_fd(file_guard.as_ref().as_raw_fd()) };
-        let guard = scopeguard::guard(file_guard, |_| {
-            panic!("must not drop future while operation is ongoing (todo: pass file_guard to tokio_epoll_uring to aovid this)")
-        });
-        let ((owned_fd, buf), res) = system.read(owned_fd, offset, buf).await;
-        let _ = OwnedFd::into_raw_fd(owned_fd);
-        let _ = scopeguard::ScopeGuard::into_inner(guard);
+        let ((_, buf), res) = system.read(file_guard, offset, buf).await;
         let PageWriteGuardBuf {
             buf: write_guard,
             init_up_to,
@@ -686,9 +676,9 @@ impl VirtualFile {
     }
 
     async fn write_at(&self, buf: &[u8], offset: u64) -> Result<usize, Error> {
-        let result = with_file!(self, StorageIoOperation::Write, |file| file
-            .as_ref()
-            .write_at(buf, offset));
+        let result = with_file!(self, StorageIoOperation::Write, |file_guard| {
+            file_guard.with_std_file(|std_file| std_file.write_at(buf, offset))
+        });
         if let Ok(size) = result {
             STORAGE_IO_SIZE
                 .with_label_values(&["write", &self.tenant_id, &self.timeline_id])
@@ -702,14 +692,36 @@ struct FileGuard<'a> {
     slot_guard: RwLockReadGuard<'a, SlotInner>,
 }
 
-impl<'a> AsRef<File> for FileGuard<'a> {
-    fn as_ref(&self) -> &File {
+impl<'a> AsRef<OwnedFd> for FileGuard<'a> {
+    fn as_ref(&self) -> &OwnedFd {
         // This unwrap is safe because we only create `FileGuard`s
         // if we know that the file is Some.
         self.slot_guard.file.as_ref().unwrap()
     }
 }
 
+impl<'a> FileGuard<'a> {
+    // TODO: switch to tokio-epoll-uring native operations.
+    #[deprecated]
+    fn with_std_file<F, R>(&mut self, with: F) -> R
+    where
+        F: FnOnce(&mut File) -> R,
+    {
+        // SAFETY:
+        // - lifetime of the fd: `file` doesn't outlive the OwnedFd stored in `self`.
+        // - &mut usage below: `self` is `&mut`, hence this call is the only task/thread that has control over the underlying fd
+        let mut file = unsafe { File::from_raw_fd(self.as_ref().as_raw_fd()) };
+        with(&mut file)
+    }
+}
+
+impl tokio_epoll_uring::IoFd for FileGuard<'static> {
+    unsafe fn as_fd(&self) -> RawFd {
+        let owned_fd: &OwnedFd = self.as_ref();
+        owned_fd.as_raw_fd()
+    }
+}
+
 #[cfg(test)]
 impl VirtualFile {
     pub(crate) async fn read_blk(