diff --git a/backend/endpoints/roms/__init__.py b/backend/endpoints/roms/__init__.py
index 6374a4436..06f2407b0 100644
--- a/backend/endpoints/roms/__init__.py
+++ b/backend/endpoints/roms/__init__.py
@@ -868,6 +868,12 @@ async def head_rom_content(
         files = [f for f in files if f.id in file_id_values]
     files.sort(key=lambda x: x.file_name)
 
+    if not files:
+        raise HTTPException(
+            status_code=status.HTTP_404_NOT_FOUND,
+            detail=f"No files found for ROM {id}",
+        )
+
     # Serve the file directly in development mode for emulatorjs
     if DEV_MODE:
         if len(files) == 1:
@@ -945,6 +951,12 @@ async def get_rom_content(
         files = [f for f in files if f.id in file_id_values]
     files.sort(key=lambda x: x.file_name)
 
+    if not files:
+        raise HTTPException(
+            status_code=status.HTTP_404_NOT_FOUND,
+            detail=f"No files found for ROM {id}",
+        )
+
     log.info(
         f"User {hl(current_username, color=BLUE)} is downloading {hl(rom.fs_name)}"
     )
diff --git a/backend/tests/conftest.py b/backend/tests/conftest.py
index 26dd58512..c44efeee1 100644
--- a/backend/tests/conftest.py
+++ b/backend/tests/conftest.py
@@ -89,6 +89,18 @@ def rom(admin_user: User, platform: Platform):
     return rom
 
 
+@pytest.fixture
+def rom_file(rom: Rom):
+    """A single content file attached to the `rom` fixture."""
+    rom_file = RomFile(
+        rom_id=rom.id,
+        file_name="test_rom.zip",
+        file_path=rom.fs_path,
+        file_size_bytes=1000,
+    )
+    return db_rom_handler.add_rom_file(rom_file)
+
+
 @pytest.fixture
 def multi_file_rom(admin_user: User, platform: Platform):
     """A ROM stored as a game folder with multiple files (e.g. multi-disc).
diff --git a/backend/tests/endpoints/roms/test_rom.py b/backend/tests/endpoints/roms/test_rom.py
index b0c06f59e..d7193f364 100644
--- a/backend/tests/endpoints/roms/test_rom.py
+++ b/backend/tests/endpoints/roms/test_rom.py
@@ -82,6 +82,62 @@ def test_get_all_roms(
     assert items[0]["id"] == rom.id
 
 
+def test_get_rom_content_requires_auth(client: TestClient, rom: Rom, rom_file):
+    response = client.get(f"/api/roms/{rom.id}/content/test_rom.zip")
+    assert response.status_code == status.HTTP_403_FORBIDDEN
+
+
+def test_get_rom_content_single_file(
+    client: TestClient, access_token: str, rom: Rom, rom_file
+):
+    response = client.get(
+        f"/api/roms/{rom.id}/content/test_rom.zip",
+        headers={"Authorization": f"Bearer {access_token}"},
+        follow_redirects=False,
+    )
+    assert response.status_code == status.HTTP_200_OK
+    # Single-file roms are proxied through nginx via X-Accel-Redirect.
+    assert "X-Accel-Redirect" in response.headers
+
+
+def test_get_rom_content_valid_file_id(
+    client: TestClient, access_token: str, rom: Rom, rom_file
+):
+    response = client.get(
+        f"/api/roms/{rom.id}/content/test_rom.zip",
+        headers={"Authorization": f"Bearer {access_token}"},
+        params={"file_ids": str(rom_file.id)},
+        follow_redirects=False,
+    )
+    assert response.status_code == status.HTTP_200_OK
+    assert "X-Accel-Redirect" in response.headers
+
+
+def test_get_rom_content_stale_file_id_returns_404(
+    client: TestClient, access_token: str, rom: Rom, rom_file
+):
+    # Regression test for #3470: a remembered file id that no longer exists
+    # (e.g. after a rename gave the file a new id) must return a clean 404
+    # instead of an empty-.m3u ZIP that nginx aborts as a 0-byte response.
+    stale_file_id = rom_file.id + 999
+    response = client.get(
+        f"/api/roms/{rom.id}/content/test_rom.zip",
+        headers={"Authorization": f"Bearer {access_token}"},
+        params={"file_ids": str(stale_file_id)},
+        follow_redirects=False,
+    )
+    assert response.status_code == status.HTTP_404_NOT_FOUND
+
+
+def test_get_rom_content_missing_rom_returns_404(client: TestClient, access_token: str):
+    response = client.get(
+        "/api/roms/999999/content/missing.zip",
+        headers={"Authorization": f"Bearer {access_token}"},
+        follow_redirects=False,
+    )
+    assert response.status_code == status.HTTP_404_NOT_FOUND
+
+
 @patch.object(FSRomsHandler, "rename_fs_rom")
 @patch.object(IGDBHandler, "get_rom_by_id", return_value=IGDBRom(igdb_id=None))
 def test_update_rom(