diff --git a/src/Entries/UpdateStructuredEntryOrderAndParent.php b/src/Entries/UpdateStructuredEntryOrderAndParent.php
index bd7a5624518..623da3707bb 100644
--- a/src/Entries/UpdateStructuredEntryOrderAndParent.php
+++ b/src/Entries/UpdateStructuredEntryOrderAndParent.php
@@ -16,12 +16,14 @@ public function handle(CollectionTreeSaved $event)
         $moved = $diff->moved();
         $ids = array_merge($moved, $diff->added());
 
-        if (empty($ids)) {
-            return;
+        if (! empty($ids)) {
+            $collection->updateEntryParent($ids);
         }
 
-        $collection->updateEntryParent($ids);
-        $collection->updateEntryOrder($this->idsWithDescendants($tree, $moved, $ids));
+        // Moved entries and their descendants are kept since stale references in the raw tree can hide their shift.
+        if ($orderIds = $this->idsWithDescendants($tree, $moved, array_merge($moved, $diff->orderChanged()))) {
+            $collection->updateEntryOrder($orderIds);
+        }
     }
 
     private function idsWithDescendants(CollectionTree $tree, array $moved, array $ids): array
diff --git a/src/Stache/Stores/CollectionEntriesStore.php b/src/Stache/Stores/CollectionEntriesStore.php
index 09109f073da..41a293e34d7 100644
--- a/src/Stache/Stores/CollectionEntriesStore.php
+++ b/src/Stache/Stores/CollectionEntriesStore.php
@@ -275,10 +275,15 @@ private function updateEntriesWithinIndex($index, $ids)
             return $index->update();
         }
 
+        // Write the index to the cache once, rather than once per entry like updateItem() does.
+        $index->load();
+
         collect($ids)
             ->map(fn ($id) => Entry::find($id))
             ->filter()
-            ->each(fn ($entry) => $index->updateItem($entry));
+            ->each(fn ($entry) => $index->put($this->getItemKey($entry), $index->getItemValue($entry)));
+
+        $index->cache();
     }
 
     private function updateEntriesWithinStore($ids)
diff --git a/src/Structures/CollectionTreeDiff.php b/src/Structures/CollectionTreeDiff.php
index ba907b9022c..f74a9712552 100644
--- a/src/Structures/CollectionTreeDiff.php
+++ b/src/Structures/CollectionTreeDiff.php
@@ -8,6 +8,7 @@ class CollectionTreeDiff
     protected $removed = [];
     protected $moved = [];
     protected $ancestryChanged = [];
+    protected $orderChanged = [];
     protected $expectsRoot = false;
     private $positions;
 
@@ -25,6 +26,7 @@ public function analyze($old, $new, $expectsRoot = false)
         $this->removed = $old->keys()->diff($new->keys())->values()->all();
         $this->moved = $this->analyzeMoved();
         $this->ancestryChanged = $this->analyzeAncestryChanges();
+        $this->orderChanged = $this->analyzeOrderChanges($old, $new);
 
         return $this;
     }
@@ -105,6 +107,15 @@ public function ancestryChanged()
         return $this->ancestryChanged;
     }
 
+    /**
+     * Items whose position in the flattened tree, and so their "order", has changed.
+     * Unlike moved(), this includes items shifted by changes elsewhere in the tree.
+     */
+    public function orderChanged()
+    {
+        return $this->orderChanged;
+    }
+
     private function preparePositions($old, $new)
     {
         $positions = [];
@@ -137,4 +148,11 @@ private function analyzeAncestryChanges()
             return $item[0]['path'] !== $item[1]['path'];
         })->keys()->all();
     }
+
+    private function analyzeOrderChanges($old, $new)
+    {
+        $oldOrder = $old->keys()->flip();
+
+        return $new->keys()->filter(fn ($id, $i) => $oldOrder->get($id) !== $i)->values()->all();
+    }
 }
diff --git a/tests/Data/Structures/CollectionTreeTest.php b/tests/Data/Structures/CollectionTreeTest.php
index 57e9f9ca816..91858dc9296 100644
--- a/tests/Data/Structures/CollectionTreeTest.php
+++ b/tests/Data/Structures/CollectionTreeTest.php
@@ -3,6 +3,7 @@
 namespace Tests\Data\Structures;
 
 use Facades\Tests\Factories\EntryFactory;
+use Illuminate\Support\Arr;
 use Illuminate\Support\Facades\Event;
 use PHPUnit\Framework\Attributes\Test;
 use Statamic\Events\CollectionTreeEntriesMovedOrRemoved;
@@ -320,6 +321,61 @@ public function reordering_a_parent_keeps_the_order_index_of_its_descendants_in_
         ], $this->cachedOrderIndex('pages'));
     }
 
+    #[Test]
+    public function entries_shifted_by_a_tree_change_keep_their_order_index_in_sync()
+    {
+        $collection = tap(Collection::make('pages')->routes('{slug}')->structureContents(['root' => false]))->save();
+
+        foreach (['alfa', 'a1', 'a2', 'bravo', 'b1'] as $id) {
+            EntryFactory::collection('pages')->id($id)->slug($id)->data(['title' => $id])->create();
+        }
+
+        $collection->structure()->in('en')->tree([
+            ['entry' => 'alfa', 'children' => [
+                ['entry' => 'a1'],
+            ]],
+            ['entry' => 'bravo', 'children' => [
+                ['entry' => 'b1'],
+            ]],
+        ])->save();
+
+        // Adding "a2" shifts "bravo" and "b1" without changing their parent or index.
+        $collection->structure()->in('en')->tree([
+            ['entry' => 'alfa', 'children' => [
+                ['entry' => 'a1'],
+                ['entry' => 'a2'],
+            ]],
+            ['entry' => 'bravo', 'children' => [
+                ['entry' => 'b1'],
+            ]],
+        ])->save();
+
+        $this->assertEquals([
+            'alfa' => 1,
+            'a1' => 2,
+            'a2' => 3,
+            'bravo' => 4,
+            'b1' => 5,
+        ], $this->cachedOrderIndex('pages'));
+
+        // Removing "a2" shifts them back, with nothing moved or added.
+        $collection->structure()->in('en')->tree([
+            ['entry' => 'alfa', 'children' => [
+                ['entry' => 'a1'],
+            ]],
+            ['entry' => 'bravo', 'children' => [
+                ['entry' => 'b1'],
+            ]],
+        ])->save();
+
+        $this->assertEquals([
+            'alfa' => 1,
+            'a1' => 2,
+            'bravo' => 3,
+            'b1' => 4,
+        ], Arr::except($this->cachedOrderIndex('pages'), 'a2'));
+    }
+
     private function cachedOrderIndex(string $collection): array
     {
         return Stache::store('entries')->store($collection)->index('order')->items()->all();