diff --git a/zerver/lib/storage.py b/zerver/lib/storage.py
index 0465ae69a8..8ca7f66e1f 100644
--- a/zerver/lib/storage.py
+++ b/zerver/lib/storage.py
@@ -24,26 +24,62 @@ else:
         return os.path.join(settings.STATIC_ROOT, path)
 
 
-def reformat_medium_filename(hashed_name: str) -> str:
-    """
-    Because the protocol for getting medium-size avatar URLs
-    was never fully documented, the mobile apps use a
-    substitution of the form s/.png/-medium.png/ to get the
-    medium-size avatar URLs. Thus, we must ensure the hashed
-    filenames for system bot avatars follow this naming convention.
-    """
-
-    name_parts = hashed_name.rsplit(".", 1)
-    base_name = name_parts[0]
-
-    if len(name_parts) != 2 or "-medium" not in base_name:
-        return hashed_name
-    extension = name_parts[1].replace("png", "medium.png")
-    base_name = base_name.replace("-medium", "")
-    return f"{base_name}-{extension}"
-
-
 class IgnoreBundlesManifestStaticFilesStorage(ManifestStaticFilesStorage):
+    hashed_static_avatar_file_map: dict[str, str] = {}
+
+    def process_static_avatars_name(
+        self,
+        name: str,
+        content: Optional["File[bytes]"] = None,
+        filename: str | None = None,
+    ) -> str:
+        """
+        Because the protocol for getting medium-size avatar URLs
+        was never fully documented, the mobile apps use a
+        substitution of the form s/.png/-medium.png/ to get the
+        medium-size avatar URLs.
+
+        This function hashes system bots' avatar files in a way
+        that follows the pattern used for user-uploaded avatars.
+
+        It ensures the following:
+
+            * Hashed filenames for system bot avatars follow this
+            naming convention:
+            - avatar.png -> avatar-medium.png
+
+            * The system bots' default avatar file and its medium
+            version share the same hash:
+            - bot.36f721bad3d0.png -> bot.36f721bad3d0-medium.png
+        """
+
+        def reformat_medium_filename(hashed_name: str) -> str:
+            name_parts = hashed_name.rsplit(".", 1)
+            base_name = name_parts[0]
+
+            if len(name_parts) != 2 or "-medium" not in base_name:
+                return hashed_name
+            extension = name_parts[1].replace("png", "medium.png")
+            base_name = base_name.replace("-medium", "")
+            return f"{base_name}-{extension}"
+
+        if name.endswith("-medium.png"):
+            # This logic relies on the fact that the medium files will
+            # be hashed first due to the "-medium" string, which places
+            # them earlier in the naming order. So, adhering to the
+            # medium file naming convention is crucial for this logic.
+            hashed_medium_file: str = reformat_medium_filename(
+                super().hashed_name(name, content, filename)
+            )
+
+            default_file = name.replace("-medium.png", ".png")
+            hashed_default_file = hashed_medium_file.replace("-medium.png", ".png")
+
+            self.hashed_static_avatar_file_map[default_file] = hashed_default_file
+            return hashed_medium_file
+        assert name in self.hashed_static_avatar_file_map
+        return self.hashed_static_avatar_file_map[name]
+
     @override
     def hashed_name(
         self, name: str, content: Optional["File[bytes]"] = None, filename: str | None = None
@@ -64,11 +100,8 @@ class IgnoreBundlesManifestStaticFilesStorage(ManifestStaticFilesStorage):
             # so they can hit our Nginx caching block for static files.
             # We don't need to worry about stale caches since these are
             # only used by the system bots.
-            if not name.endswith("-medium.png"):
-                return super().hashed_name(name, content, filename)
+            return self.process_static_avatars_name(name, content, filename)
 
-            hashed_medium_file = super().hashed_name(name, content, filename)
-            return reformat_medium_filename(hashed_medium_file)
         if name == "generated/emoji/emoji_api.json":
             # Unlike most .json files, we do want to hash this file;
             # its hashed URL is returned as part of the API.  See