diff --git a/pageserver/src/layered_repository.rs b/pageserver/src/layered_repository.rs
index 080ac2852d..59e73d961d 100644
--- a/pageserver/src/layered_repository.rs
+++ b/pageserver/src/layered_repository.rs
@@ -1432,7 +1432,8 @@ impl LayeredTimeline {
 
             let layers = timeline.layers.read().unwrap();
 
-            // Check the open and frozen in-memory layers first
+            // Check the open and frozen in-memory layers first, in order from newest
+            // to oldest.
             if let Some(open_layer) = &layers.open_layer {
                 let start_lsn = open_layer.get_lsn_range().start;
                 if cont_lsn > start_lsn {
@@ -1450,7 +1451,7 @@ impl LayeredTimeline {
                     continue;
                 }
             }
-            for frozen_layer in layers.frozen_layers.iter() {
+            for frozen_layer in layers.frozen_layers.iter().rev() {
                 let start_lsn = frozen_layer.get_lsn_range().start;
                 if cont_lsn > start_lsn {
                     //info!("CHECKING for {} at {} on frozen layer {}", key, cont_lsn, frozen_layer.filename().display());
@@ -1695,7 +1696,9 @@ impl LayeredTimeline {
             self.conf.timeline_path(&self.timelineid, &self.tenantid),
         ])?;
 
-        // Finally, replace the frozen in-memory layer with the new on-disk layers
+        fail_point!("flush-frozen");
+
+        // Finally, replace the frozen in-memory layer with the new on-disk layer
         {
             let mut layers = self.layers.write().unwrap();
             let l = layers.frozen_layers.pop_front();
diff --git a/pageserver/src/layered_repository/layer_map.rs b/pageserver/src/layered_repository/layer_map.rs
index 03ee8b8ef1..91a900dde0 100644
--- a/pageserver/src/layered_repository/layer_map.rs
+++ b/pageserver/src/layered_repository/layer_map.rs
@@ -43,10 +43,13 @@ pub struct LayerMap {
     pub next_open_layer_at: Option<Lsn>,
 
     ///
-    /// The frozen layer, if any, contains WAL older than the current 'open_layer'
-    /// or 'next_open_layer_at', but newer than any historic layer. The frozen
-    /// layer is during checkpointing, when an InMemoryLayer is being written out
-    /// to disk.
+    /// Frozen layers, if any. Frozen layers are in-memory layers that
+    /// are no longer added to, but haven't been written out to disk
+    /// yet. They contain WAL older than the current 'open_layer' or
+    /// 'next_open_layer_at', but newer than any historic layer.
+    /// The frozen layers are in order from oldest to newest, so that
+    /// the newest one is in the 'back' of the VecDeque, and the oldest
+    /// in the 'front'.
     ///
     pub frozen_layers: VecDeque<Arc<InMemoryLayer>>,
 
diff --git a/test_runner/batch_others/test_ancestor_branch.py b/test_runner/batch_others/test_ancestor_branch.py
index aeb45348ad..75fe3cde0f 100644
--- a/test_runner/batch_others/test_ancestor_branch.py
+++ b/test_runner/batch_others/test_ancestor_branch.py
@@ -33,6 +33,10 @@ def test_ancestor_branch(zenith_env_builder: ZenithEnvBuilder):
             'compaction_target_size': '4194304',
         })
 
+    with closing(env.pageserver.connect()) as psconn:
+        with psconn.cursor(cursor_factory=psycopg2.extras.DictCursor) as pscur:
+            pscur.execute("failpoints flush-frozen=sleep(10000)")
+
     env.zenith_cli.create_timeline(f'main', tenant_id=tenant)
     pg_branch0 = env.postgres.create_start('main', tenant_id=tenant)
     branch0_cur = pg_branch0.connect().cursor()