diff --git a/synapse/rest/media/v1/media_repository.py b/synapse/rest/media/v1/media_repository.py
index a0162d4255..3375455c43 100644
--- a/synapse/rest/media/v1/media_repository.py
+++ b/synapse/rest/media/v1/media_repository.py
@@ -509,7 +509,7 @@ class MediaRepository:
         t_height: int,
         t_method: str,
         t_type: str,
-        url_cache: str,
+        url_cache: Optional[str],
     ) -> Optional[str]:
         input_path = await self.media_storage.ensure_media_is_in_local_cache(
             FileInfo(None, media_id, url_cache=url_cache)
diff --git a/synapse/rest/media/v1/thumbnail_resource.py b/synapse/rest/media/v1/thumbnail_resource.py
index d653a58be9..c345ec6498 100644
--- a/synapse/rest/media/v1/thumbnail_resource.py
+++ b/synapse/rest/media/v1/thumbnail_resource.py
@@ -114,6 +114,7 @@ class ThumbnailResource(DirectServeJsonResource):
             m_type,
             thumbnail_infos,
             media_id,
+            media_id,
             url_cache=media_info["url_cache"],
             server_name=None,
         )
@@ -269,6 +270,7 @@ class ThumbnailResource(DirectServeJsonResource):
             method,
             m_type,
             thumbnail_infos,
+            media_id,
             media_info["filesystem_id"],
             url_cache=None,
             server_name=server_name,
@@ -282,6 +284,7 @@ class ThumbnailResource(DirectServeJsonResource):
         desired_method: str,
         desired_type: str,
         thumbnail_infos: List[Dict[str, Any]],
+        media_id: str,
         file_id: str,
         url_cache: Optional[str] = None,
         server_name: Optional[str] = None,
@@ -316,9 +319,53 @@ class ThumbnailResource(DirectServeJsonResource):
                 respond_404(request)
                 return
 
+            responder = await self.media_storage.fetch_media(file_info)
+            if responder:
+                await respond_with_responder(
+                    request,
+                    responder,
+                    file_info.thumbnail_type,
+                    file_info.thumbnail_length,
+                )
+                return
+
+            # If we can't find the thumbnail we regenerate it. This can happen
+            # if e.g. we've deleted the thumbnails but still have the original
+            # image somewhere.
+            #
+            # Since we have an entry for the thumbnail in the DB we a) know we
+            # have have successfully generated the thumbnail in the past (so we
+            # don't need to worry about repeatedly failing to generate
+            # thumbnails), and b) have already calculated that appropriate
+            # width/height/method so we can just call the "generate exact"
+            # methods.
+
+            if server_name:
+                await self.media_repo.generate_remote_exact_thumbnail(
+                    server_name,
+                    file_id=file_id,
+                    media_id=media_id,
+                    t_width=file_info.thumbnail_width,
+                    t_height=file_info.thumbnail_height,
+                    t_method=file_info.thumbnail_method,
+                    t_type=file_info.thumbnail_type,
+                )
+            else:
+                await self.media_repo.generate_local_exact_thumbnail(
+                    media_id=media_id,
+                    t_width=file_info.thumbnail_width,
+                    t_height=file_info.thumbnail_height,
+                    t_method=file_info.thumbnail_method,
+                    t_type=file_info.thumbnail_type,
+                    url_cache=url_cache,
+                )
+
             responder = await self.media_storage.fetch_media(file_info)
             await respond_with_responder(
-                request, responder, file_info.thumbnail_type, file_info.thumbnail_length
+                request,
+                responder,
+                file_info.thumbnail_type,
+                file_info.thumbnail_length,
             )
         else:
             logger.info("Failed to find any generated thumbnails")
diff --git a/synapse/storage/databases/main/media_repository.py b/synapse/storage/databases/main/media_repository.py
index a0313c3ccf..9ee642c668 100644
--- a/synapse/storage/databases/main/media_repository.py
+++ b/synapse/storage/databases/main/media_repository.py
@@ -344,16 +344,16 @@ class MediaRepositoryStore(MediaRepositoryBackgroundUpdateStore):
         thumbnail_method,
         thumbnail_length,
     ):
-        await self.db_pool.simple_insert(
-            "local_media_repository_thumbnails",
-            {
+        await self.db_pool.simple_upsert(
+            table="local_media_repository_thumbnails",
+            keyvalues={
                 "media_id": media_id,
                 "thumbnail_width": thumbnail_width,
                 "thumbnail_height": thumbnail_height,
                 "thumbnail_method": thumbnail_method,
                 "thumbnail_type": thumbnail_type,
-                "thumbnail_length": thumbnail_length,
             },
+            values={"thumbnail_length": thumbnail_length},
             desc="store_local_thumbnail",
         )
 
@@ -498,18 +498,18 @@ class MediaRepositoryStore(MediaRepositoryBackgroundUpdateStore):
         thumbnail_method,
         thumbnail_length,
     ):
-        await self.db_pool.simple_insert(
-            "remote_media_cache_thumbnails",
-            {
+        await self.db_pool.simple_upsert(
+            table="remote_media_cache_thumbnails",
+            keyvalues={
                 "media_origin": origin,
                 "media_id": media_id,
                 "thumbnail_width": thumbnail_width,
                 "thumbnail_height": thumbnail_height,
                 "thumbnail_method": thumbnail_method,
                 "thumbnail_type": thumbnail_type,
-                "thumbnail_length": thumbnail_length,
-                "filesystem_id": filesystem_id,
             },
+            values={"thumbnail_length": thumbnail_length},
+            insertion_values={"filesystem_id": filesystem_id},
             desc="store_remote_media_thumbnail",
         )