diff --git a/zerver/tests/test_thumbnail.py b/zerver/tests/test_thumbnail.py
index affb060d36..9a3cb70975 100644
--- a/zerver/tests/test_thumbnail.py
+++ b/zerver/tests/test_thumbnail.py
@@ -1,4 +1,6 @@
 import re
+from collections.abc import Iterator
+from contextlib import contextmanager
 from dataclasses import asdict
 from io import StringIO
 from unittest.mock import patch
@@ -469,3 +471,136 @@ class TestStoreThumbnail(ZulipTestCase):
             "zerver.lib.thumbnail.THUMBNAIL_OUTPUT_FORMATS", [still_webp, anim_webp, still_jpeg]
         ):
             self.assertEqual(missing_thumbnails(image_attachment), [anim_webp, still_jpeg])
+
+
+class TestThumbnailRetrieval(ZulipTestCase):
+    @contextmanager
+    def mock_formats(self, thumbnail_formats: list[ThumbnailFormat]) -> Iterator[None]:
+        with (
+            patch("zerver.lib.thumbnail.THUMBNAIL_OUTPUT_FORMATS", thumbnail_formats),
+            patch("zerver.views.upload.THUMBNAIL_OUTPUT_FORMATS", thumbnail_formats),
+        ):
+            yield
+
+    def test_get_thumbnail(self) -> None:
+        assert settings.LOCAL_FILES_DIR
+        hamlet = self.example_user("hamlet")
+        self.login_user(hamlet)
+
+        webp_anim = ThumbnailFormat("webp", 100, 75, animated=True)
+        webp_still = ThumbnailFormat("webp", 100, 75, animated=False)
+        with self.mock_formats([webp_anim, webp_still]):
+            with (
+                self.captureOnCommitCallbacks(execute=True),
+                get_test_image_file("animated_unequal_img.gif") as image_file,
+            ):
+                json_response = self.assert_json_success(
+                    self.client_post("/json/user_uploads", {"file": image_file})
+                )
+                path_id = re.sub(r"/user_uploads/", "", json_response["url"])
+
+                # Image itself is available immediately
+                response = self.client_get(f"/user_uploads/{path_id}")
+                self.assertEqual(response.status_code, 200)
+                self.assertEqual(response.headers["Content-Type"], "image/gif")
+
+                # Exit the block, triggering the thumbnailing worker
+
+            thumbnail_response = self.client_get(f"/user_uploads/thumbnail/{path_id}/{webp_still!s}")
+            self.assertEqual(thumbnail_response.status_code, 200)
+            self.assertEqual(thumbnail_response.headers["Content-Type"], "image/webp")
+            self.assertLess(
+                int(thumbnail_response.headers["Content-Length"]),
+                int(response.headers["Content-Length"]),
+            )
+
+            animated_response = self.client_get(f"/user_uploads/thumbnail/{path_id}/{webp_anim!s}")
+            self.assertEqual(animated_response.status_code, 200)
+            self.assertEqual(animated_response.headers["Content-Type"], "image/webp")
+            self.assertLess(
+                int(thumbnail_response.headers["Content-Length"]),
+                int(animated_response.headers["Content-Length"]),
+            )
+
+            # Invalid thumbnail format
+            response = self.client_get(f"/user_uploads/thumbnail/{path_id}/bogus")
+            self.assertEqual(response.status_code, 404)
+            self.assertEqual(response.headers["Content-Type"], "image/png")
+
+            # Format we don't have
+            response = self.client_get(f"/user_uploads/thumbnail/{path_id}/1x1.png")
+            self.assertEqual(response.status_code, 404)
+            self.assertEqual(response.headers["Content-Type"], "image/png")
+
+            # path_id for a non-image
+            with (
+                self.captureOnCommitCallbacks(execute=True),
+                get_test_image_file("text.txt") as text_file,
+            ):
+                json_response = self.assert_json_success(
+                    self.client_post("/json/user_uploads", {"file": text_file})
+                )
+                text_path_id = re.sub(r"/user_uploads/", "", json_response["url"])
+            response = self.client_get(f"/user_uploads/thumbnail/{text_path_id}/{webp_still!s}")
+            self.assertEqual(response.status_code, 404)
+            self.assertEqual(response.headers["Content-Type"], "image/png")
+
+        # Shrink the list of formats, and check that we can still get
+        # the thumbnails that were generated at the time
+        with self.mock_formats([webp_still]):
+            response = self.client_get(f"/user_uploads/thumbnail/{path_id}/{webp_still!s}")
+            self.assertEqual(response.status_code, 200)
+
+            response = self.client_get(f"/user_uploads/thumbnail/{path_id}/{webp_anim!s}")
+            self.assertEqual(response.status_code, 200)
+
+        # Grow the format list, and check that fetching that new
+        # format generates all of the missing formats
+        jpeg_still = ThumbnailFormat("jpg", 100, 75, animated=False)
+        big_jpeg_still = ThumbnailFormat("jpg", 200, 150, animated=False)
+        with (
+            self.mock_formats([webp_still, jpeg_still, big_jpeg_still]),
+            patch.object(
+                pyvips.Image, "thumbnail_buffer", wraps=pyvips.Image.thumbnail_buffer
+            ) as thumb_mock,
+        ):
+            small_response = self.client_get(f"/user_uploads/thumbnail/{path_id}/{jpeg_still!s}")
+            self.assertEqual(small_response.status_code, 200)
+            self.assertEqual(small_response.headers["Content-Type"], "image/jpeg")
+            # This made two thumbnails
+            self.assertEqual(thumb_mock.call_count, 2)
+
+            thumb_mock.reset_mock()
+            big_response = self.client_get(f"/user_uploads/thumbnail/{path_id}/{big_jpeg_still!s}")
+            self.assertEqual(big_response.status_code, 200)
+            self.assertEqual(big_response.headers["Content-Type"], "image/jpeg")
+            thumb_mock.assert_not_called()
+
+            self.assertLess(
+                int(small_response.headers["Content-Length"]),
+                int(big_response.headers["Content-Length"]),
+            )
+
+        # Upload a static image, and verify that we only generate the still versions
+        with self.mock_formats([webp_anim, webp_still, jpeg_still]):
+            with (
+                self.captureOnCommitCallbacks(execute=True),
+                get_test_image_file("img.tif") as image_file,
+            ):
+                json_response = self.assert_json_success(
+                    self.client_post("/json/user_uploads", {"file": image_file})
+                )
+                path_id = re.sub(r"/user_uploads/", "", json_response["url"])
+                # Exit the block, triggering the thumbnailing worker
+
+            response = self.client_get(f"/user_uploads/thumbnail/{path_id}/{webp_still!s}")
+            self.assertEqual(response.status_code, 200)
+            self.assertEqual(response.headers["Content-Type"], "image/webp")
+
+            response = self.client_get(f"/user_uploads/thumbnail/{path_id}/{webp_anim!s}")
+            self.assertEqual(response.status_code, 404)
+            self.assertEqual(response.headers["Content-Type"], "image/png")
+
+            response = self.client_get(f"/user_uploads/thumbnail/{path_id}/{jpeg_still!s}")
+            self.assertEqual(response.status_code, 200)
+            self.assertEqual(response.headers["Content-Type"], "image/jpeg")
diff --git a/zerver/views/upload.py b/zerver/views/upload.py
index faf5f85df7..b8fc646e6f 100644
--- a/zerver/views/upload.py
+++ b/zerver/views/upload.py
@@ -8,6 +8,7 @@ from django.conf import settings
 from django.contrib.auth.models import AnonymousUser
 from django.core.files.uploadedfile import UploadedFile
 from django.core.signing import BadSignature, TimestampSigner
+from django.db import transaction
 from django.http import (
     FileResponse,
     HttpRequest,
@@ -29,15 +30,22 @@ from zerver.lib.exceptions import JsonableError
 from zerver.lib.mime_types import guess_type
 from zerver.lib.response import json_success
 from zerver.lib.storage import static_path
+from zerver.lib.thumbnail import (
+    THUMBNAIL_OUTPUT_FORMATS,
+    BaseThumbnailFormat,
+    StoredThumbnailFormat,
+)
 from zerver.lib.upload import (
     check_upload_within_quota,
+    get_image_thumbnail_path,
     get_public_upload_root_url,
     upload_message_attachment_from_request,
 )
 from zerver.lib.upload.base import INLINE_MIME_TYPES
 from zerver.lib.upload.local import assert_is_local_storage_path
 from zerver.lib.upload.s3 import get_signed_upload_url
-from zerver.models import UserProfile
+from zerver.models import ImageAttachment, UserProfile
+from zerver.worker.thumbnail import ensure_thumbnails
 
 
 def patch_disposition_header(response: HttpResponse, url: str, is_attachment: bool) -> None:
@@ -155,8 +163,16 @@ def serve_file_backend(
     maybe_user_profile: UserProfile | AnonymousUser,
     realm_id_str: str,
     filename: str,
+    thumbnail_format: str | None = None,
 ) -> HttpResponseBase:
-    return serve_file(request, maybe_user_profile, realm_id_str, filename, url_only=False)
+    return serve_file(
+        request,
+        maybe_user_profile,
+        realm_id_str,
+        filename,
+        url_only=False,
+        thumbnail_format=thumbnail_format,
+    )
 
 
 def serve_file_url_backend(
@@ -192,6 +208,7 @@ def serve_file(
     maybe_user_profile: UserProfile | AnonymousUser,
     realm_id_str: str,
     filename: str,
+    thumbnail_format: str | None = None,
     url_only: bool = False,
     force_download: bool = False,
 ) -> HttpResponseBase:
@@ -227,6 +244,50 @@ def serve_file(
         url = generate_unauthed_file_access_url(path_id)
         return json_success(request, data=dict(url=url))
 
+    if thumbnail_format is not None:
+        # Check if this is something that we thumbnail at all
+        try:
+            image_attachment = ImageAttachment.objects.get(path_id=path_id)
+        except ImageAttachment.DoesNotExist:
+            return serve_image_error(404, "images/errors/image-not-exist.png")
+
+        # Validate that this is a potential thumbnail format
+        requested_format = BaseThumbnailFormat.from_string(thumbnail_format)
+        if requested_format is None:
+            return serve_image_error(404, "images/errors/image-not-exist.png")
+
+        rendered_formats = [StoredThumbnailFormat(**f) for f in image_attachment.thumbnail_metadata]
+
+        # We never generate animated versions if the input was still,
+        # so filter those out
+        if image_attachment.frames == 1:
+            potential_output_formats = [
+                thumbnail_format
+                for thumbnail_format in THUMBNAIL_OUTPUT_FORMATS
+                if not thumbnail_format.animated
+            ]
+        else:
+            potential_output_formats = THUMBNAIL_OUTPUT_FORMATS
+        if requested_format not in potential_output_formats:
+            if requested_format in rendered_formats:
+                # Not a _current_ format, but we did render it at the time, so fine to serve
+                pass
+            else:
+                return serve_image_error(404, "images/errors/image-not-exist.png")
+        elif requested_format not in rendered_formats:
+            # They requested a valid format, but one we've not
+            # rendered yet.  Take a lock on the row, then render every
+            # missing format, synchronously.  The lock prevents us
+            # from doing double-work if the background worker is
+            # currently processing the row.
+            with transaction.atomic(savepoint=False):
+                ensure_thumbnails(
+                    ImageAttachment.objects.select_for_update().get(id=image_attachment.id)
+                )
+
+        # Update the path that we are fetching to be the thumbnail
+        path_id = get_image_thumbnail_path(image_attachment, requested_format)
+
     if settings.LOCAL_UPLOADS_DIR is not None:
         return serve_local(request, path_id, force_download=force_download)
     else:
diff --git a/zerver/worker/thumbnail.py b/zerver/worker/thumbnail.py
index 8e8cc05ba6..b887c4672b 100644
--- a/zerver/worker/thumbnail.py
+++ b/zerver/worker/thumbnail.py
@@ -24,6 +24,11 @@ class ThumbnailWorker(QueueProcessingWorker):
         start = time.time()
         with transaction.atomic(savepoint=False):
             try:
+                # This lock prevents us from racing with the on-demand
+                # rendering that can be triggered if a request is made
+                # directly to a thumbnail URL we have not made yet.
+                # This may mean that we may generate 0 thumbnail
+                # images once we get the lock.
                 row = ImageAttachment.objects.select_for_update().get(id=event["id"])
             except ImageAttachment.DoesNotExist:  # nocoverage
                 logger.info("ImageAttachment row %d missing", event["id"])
diff --git a/zproject/urls.py b/zproject/urls.py
index a7bed3f157..e24ec43036 100644
--- a/zproject/urls.py
+++ b/zproject/urls.py
@@ -657,6 +657,10 @@ urls += [
         "user_uploads/download/<realm_id_str>/<path:filename>",
         GET=(serve_file_download_backend, {"override_api_url_scheme", "allow_anonymous_user_web"}),
     ),
+    rest_path(
+        "user_uploads/thumbnail/<realm_id_str>/<path:filename>/<str:thumbnail_format>",
+        GET=(serve_file_backend, {"override_api_url_scheme", "allow_anonymous_user_web"}),
+    ),
     rest_path(
         "user_uploads/<realm_id_str>/<path:filename>",
         GET=(serve_file_backend, {"override_api_url_scheme", "allow_anonymous_user_web"}),