diff --git a/pageserver/src/pgdatadir_mapping.rs b/pageserver/src/pgdatadir_mapping.rs
index 65f8ddaab4..024e66d112 100644
--- a/pageserver/src/pgdatadir_mapping.rs
+++ b/pageserver/src/pgdatadir_mapping.rs
@@ -36,6 +36,8 @@ use tracing::{debug, trace, warn};
 use utils::bin_ser::DeserializeError;
 use utils::{bin_ser::BeSer, lsn::Lsn};
 
+const MAX_AUX_FILE_DELTAS: usize = 1024;
+
 #[derive(Debug)]
 pub enum LsnForTimestamp {
     /// Found commits both before and after the given timestamp
@@ -157,7 +159,6 @@ impl Timeline {
             pending_updates: HashMap::new(),
             pending_deletions: Vec::new(),
             pending_nblocks: 0,
-            pending_aux_files: None,
             pending_directory_entries: Vec::new(),
             lsn,
         }
@@ -873,11 +874,6 @@ pub struct DatadirModification<'a> {
     pending_deletions: Vec<(Range<Key>, Lsn)>,
     pending_nblocks: i64,
 
-    // If we already wrote any aux file changes in this modification, stash the latest dir.  If set,
-    // [`Self::put_file`] may assume that it is safe to emit a delta rather than checking
-    // if AUX_FILES_KEY is already set.
-    pending_aux_files: Option<AuxFilesDirectory>,
-
     /// For special "directory" keys that store key-value maps, track the size of the map
     /// if it was updated in this modification.
     pending_directory_entries: Vec<(DirectoryKind, usize)>,
@@ -1401,19 +1397,28 @@ impl<'a> DatadirModification<'a> {
             Some(Bytes::copy_from_slice(content))
         };
 
-        let dir = if let Some(mut dir) = self.pending_aux_files.take() {
+        let n_files;
+        let mut aux_files = self.tline.aux_files.lock().await;
+        if let Some(mut dir) = aux_files.dir.take() {
             // We already updated aux files in `self`: emit a delta and update our latest value
-
-            self.put(
-                AUX_FILES_KEY,
-                Value::WalRecord(NeonWalRecord::AuxFile {
-                    file_path: file_path.clone(),
-                    content: content.clone(),
-                }),
-            );
-
-            dir.upsert(file_path, content);
-            dir
+            dir.upsert(file_path.clone(), content.clone());
+            n_files = dir.files.len();
+            if aux_files.n_deltas == MAX_AUX_FILE_DELTAS {
+                self.put(
+                    AUX_FILES_KEY,
+                    Value::Image(Bytes::from(
+                        AuxFilesDirectory::ser(&dir).context("serialize")?,
+                    )),
+                );
+                aux_files.n_deltas = 0;
+            } else {
+                self.put(
+                    AUX_FILES_KEY,
+                    Value::WalRecord(NeonWalRecord::AuxFile { file_path, content }),
+                );
+                aux_files.n_deltas += 1;
+            }
+            aux_files.dir = Some(dir);
         } else {
             // Check if the AUX_FILES_KEY is initialized
             match self.get(AUX_FILES_KEY, ctx).await {
@@ -1428,7 +1433,8 @@ impl<'a> DatadirModification<'a> {
                         }),
                     );
                     dir.upsert(file_path, content);
-                    dir
+                    n_files = dir.files.len();
+                    aux_files.dir = Some(dir);
                 }
                 Err(
                     e @ (PageReconstructError::AncestorStopping(_)
@@ -1455,14 +1461,14 @@ impl<'a> DatadirModification<'a> {
                             AuxFilesDirectory::ser(&dir).context("serialize")?,
                         )),
                     );
-                    dir
+                    n_files = 1;
+                    aux_files.dir = Some(dir);
                 }
             }
-        };
+        }
 
         self.pending_directory_entries
-            .push((DirectoryKind::AuxFiles, dir.files.len()));
-        self.pending_aux_files = Some(dir);
+            .push((DirectoryKind::AuxFiles, n_files));
 
         Ok(())
     }
diff --git a/pageserver/src/tenant/timeline.rs b/pageserver/src/tenant/timeline.rs
index 59a7dcd4bd..b94ad5760a 100644
--- a/pageserver/src/tenant/timeline.rs
+++ b/pageserver/src/tenant/timeline.rs
@@ -54,7 +54,7 @@ use std::{
     ops::ControlFlow,
 };
 
-use crate::pgdatadir_mapping::DirectoryKind;
+use crate::pgdatadir_mapping::{AuxFilesDirectory, DirectoryKind};
 use crate::tenant::timeline::logical_size::CurrentLogicalSize;
 use crate::tenant::{
     layer_map::{LayerMap, SearchResult},
@@ -174,6 +174,11 @@ pub struct TimelineResources {
     >,
 }
 
+pub(crate) struct AuxFilesState {
+    pub(crate) dir: Option<AuxFilesDirectory>,
+    pub(crate) n_deltas: usize,
+}
+
 pub struct Timeline {
     conf: &'static PageServerConf,
     tenant_conf: Arc<RwLock<AttachedTenantConf>>,
@@ -357,6 +362,9 @@ pub struct Timeline {
     timeline_get_throttle: Arc<
         crate::tenant::throttle::Throttle<&'static crate::metrics::tenant_throttling::TimelineGet>,
     >,
+
+    /// Keep aux directory cache to avoid it's reconstruction on each update
+    pub(crate) aux_files: tokio::sync::Mutex<AuxFilesState>,
 }
 
 pub struct WalReceiverInfo {
@@ -1693,6 +1701,11 @@ impl Timeline {
                 gc_lock: tokio::sync::Mutex::default(),
 
                 timeline_get_throttle: resources.timeline_get_throttle,
+
+                aux_files: tokio::sync::Mutex::new(AuxFilesState {
+                    dir: None,
+                    n_deltas: 0,
+                }),
             };
             result.repartition_threshold =
                 result.get_checkpoint_distance() / REPARTITION_FREQ_IN_CHECKPOINT_DISTANCE;
diff --git a/test_runner/regress/test_layer_bloating.py b/test_runner/regress/test_layer_bloating.py
index bf5834b665..2fdee89389 100644
--- a/test_runner/regress/test_layer_bloating.py
+++ b/test_runner/regress/test_layer_bloating.py
@@ -6,6 +6,7 @@ from fixtures.log_helper import log
 from fixtures.neon_fixtures import (
     NeonEnv,
     logical_replication_sync,
+    wait_for_last_flush_lsn,
 )
 from fixtures.pg_version import PgVersion
 
@@ -52,6 +53,7 @@ def test_layer_bloating(neon_simple_env: NeonEnv, vanilla_pg):
     cur.execute("select create_snapshots(10000)")
     # Wait logical replication to sync
     logical_replication_sync(vanilla_pg, endpoint)
+    wait_for_last_flush_lsn(env, endpoint, env.initial_tenant, timeline)
     time.sleep(10)
 
     # Check layer file sizes