diff --git a/changelog.d/9438.feature b/changelog.d/9438.feature
new file mode 100644
index 0000000000..a1f6be5563
--- /dev/null
+++ b/changelog.d/9438.feature
@@ -0,0 +1 @@
+Add support for regenerating thumbnails if they have been deleted but the original image is still stored.
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/media_storage.py b/synapse/rest/media/v1/media_storage.py
index 1057e638be..b1b1c9e6ec 100644
--- a/synapse/rest/media/v1/media_storage.py
+++ b/synapse/rest/media/v1/media_storage.py
@@ -244,7 +244,7 @@ class MediaStorage:
                     await consumer.wait()
                 return local_path
 
-        raise Exception("file could not be found")
+        raise NotFoundError()
 
     def _file_info_to_path(self, file_info: FileInfo) -> str:
         """Converts file_info into a relative path.
diff --git a/synapse/rest/media/v1/thumbnail_resource.py b/synapse/rest/media/v1/thumbnail_resource.py
index d653a58be9..3ab90e9f9b 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 +319,60 @@ 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.
+
+            # First let's check that we do actually have the original image
+            # still. This will throw a 404 if we don't.
+            # TODO: We should refetch the thumbnails for remote media.
+            await self.media_storage.ensure_media_is_in_local_cache(
+                FileInfo(server_name, file_id, url_cache=url_cache)
+            )
+
+            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",
         )
 
diff --git a/tests/rest/media/v1/test_media_storage.py b/tests/rest/media/v1/test_media_storage.py
index 0789b12392..36d1e6bc4a 100644
--- a/tests/rest/media/v1/test_media_storage.py
+++ b/tests/rest/media/v1/test_media_storage.py
@@ -231,9 +231,11 @@ class MediaRepoTests(unittest.HomeserverTestCase):
 
     def prepare(self, reactor, clock, hs):
 
-        self.media_repo = hs.get_media_repository_resource()
-        self.download_resource = self.media_repo.children[b"download"]
-        self.thumbnail_resource = self.media_repo.children[b"thumbnail"]
+        media_resource = hs.get_media_repository_resource()
+        self.download_resource = media_resource.children[b"download"]
+        self.thumbnail_resource = media_resource.children[b"thumbnail"]
+        self.store = hs.get_datastore()
+        self.media_repo = hs.get_media_repository()
 
         self.media_id = "example.com/12345"
 
@@ -357,6 +359,67 @@ class MediaRepoTests(unittest.HomeserverTestCase):
         """
         self._test_thumbnail("scale", None, False)
 
+    def test_thumbnail_repeated_thumbnail(self):
+        """Test that fetching the same thumbnail works, and deleting the on disk
+        thumbnail regenerates it.
+        """
+        self._test_thumbnail(
+            "scale", self.test_image.expected_scaled, self.test_image.expected_found
+        )
+
+        if not self.test_image.expected_found:
+            return
+
+        # Fetching again should work, without re-requesting the image from the
+        # remote.
+        params = "?width=32&height=32&method=scale"
+        channel = make_request(
+            self.reactor,
+            FakeSite(self.thumbnail_resource),
+            "GET",
+            self.media_id + params,
+            shorthand=False,
+            await_result=False,
+        )
+        self.pump()
+
+        self.assertEqual(channel.code, 200)
+        if self.test_image.expected_scaled:
+            self.assertEqual(
+                channel.result["body"],
+                self.test_image.expected_scaled,
+                channel.result["body"],
+            )
+
+        # Deleting the thumbnail on disk then re-requesting it should work as
+        # Synapse should regenerate missing thumbnails.
+        origin, media_id = self.media_id.split("/")
+        info = self.get_success(self.store.get_cached_remote_media(origin, media_id))
+        file_id = info["filesystem_id"]
+
+        thumbnail_dir = self.media_repo.filepaths.remote_media_thumbnail_dir(
+            origin, file_id
+        )
+        shutil.rmtree(thumbnail_dir, ignore_errors=True)
+
+        channel = make_request(
+            self.reactor,
+            FakeSite(self.thumbnail_resource),
+            "GET",
+            self.media_id + params,
+            shorthand=False,
+            await_result=False,
+        )
+        self.pump()
+
+        self.assertEqual(channel.code, 200)
+        if self.test_image.expected_scaled:
+            self.assertEqual(
+                channel.result["body"],
+                self.test_image.expected_scaled,
+                channel.result["body"],
+            )
+
     def _test_thumbnail(self, method, expected_body, expected_found):
         params = "?width=32&height=32&method=" + method
         channel = make_request(