diff --git a/backend/endpoints/roms/__init__.py b/backend/endpoints/roms/__init__.py
index cae81edc3..c2e761e13 100644
--- a/backend/endpoints/roms/__init__.py
+++ b/backend/endpoints/roms/__init__.py
@@ -1470,6 +1470,42 @@ async def delete_roms(
     }
 
 
+@protected_route(router.post, "/cleanup-missing", [Scope.ROMS_WRITE])
+async def cleanup_missing_roms(
+    request: Request,
+    platform_id: Annotated[
+        int | None,
+        Body(
+            description="Optional platform ID to restrict cleanup to a single platform.",
+            embed=True,
+        ),
+    ] = None,
+) -> dict:
+    """Enqueue a background task to delete all ROMs flagged as missing from the filesystem.
+
+    Optionally restrict the cleanup to a single platform by providing a platform_id.
+    """
+    from config import TASK_RESULT_TTL, TASK_TIMEOUT
+    from handler.redis_handler import low_prio_queue
+    from tasks.manual.cleanup_missing_roms import cleanup_missing_roms_task
+
+    job = low_prio_queue.enqueue(
+        cleanup_missing_roms_task.run,
+        kwargs={"platform_id": platform_id},
+        job_timeout=TASK_TIMEOUT,
+        result_ttl=TASK_RESULT_TTL,
+        meta={
+            "task_name": cleanup_missing_roms_task.title,
+            "task_type": cleanup_missing_roms_task.task_type.value,
+        },
+    )
+
+    return {
+        "task_id": job.get_id(),
+        "status": str(job.get_status()),
+    }
+
+
 @protected_route(
     router.put,
     "/{id}/props",
diff --git a/backend/endpoints/tasks.py b/backend/endpoints/tasks.py
index 9362d37f5..f20264b9e 100644
--- a/backend/endpoints/tasks.py
+++ b/backend/endpoints/tasks.py
@@ -32,6 +32,7 @@ from handler.redis_handler import (
     low_prio_queue,
     redis_client,
 )
+from tasks.manual.cleanup_missing_roms import cleanup_missing_roms_task
 from tasks.manual.cleanup_orphaned_resources import cleanup_orphaned_resources_task
 from tasks.scheduled.convert_images_to_webp import convert_images_to_webp_task
 from tasks.scheduled.scan_library import scan_library_task
@@ -98,6 +99,13 @@ manual_tasks: list[ManualTask] = [
             "task": cleanup_orphaned_resources_task,
         }
     ),
+    ManualTask(
+        {
+            "name": "cleanup_missing_roms",
+            "type": TaskType.CLEANUP,
+            "task": cleanup_missing_roms_task,
+        }
+    ),
 ]
 
 
diff --git a/backend/tasks/manual/cleanup_missing_roms.py b/backend/tasks/manual/cleanup_missing_roms.py
new file mode 100644
index 000000000..a89432594
--- /dev/null
+++ b/backend/tasks/manual/cleanup_missing_roms.py
@@ -0,0 +1,91 @@
+from dataclasses import dataclass
+from typing import Any
+
+from handler.database import db_rom_handler
+from handler.filesystem import fs_resource_handler
+from logger.logger import log
+from tasks.tasks import Task, TaskType, update_job_meta
+from utils.context import initialize_context
+
+
+@dataclass
+class CleanupMissingRomsStats:
+    """Statistics for missing ROMs cleanup operations."""
+
+    platform_id: int | None = None
+    roms_found: int = 0
+    roms_deleted: int = 0
+    errors: int = 0
+
+    def update(self, **kwargs) -> None:
+        for key, value in kwargs.items():
+            if hasattr(self, key):
+                setattr(self, key, value)
+
+        update_job_meta({"cleanup_stats": self.to_dict()})
+
+    def to_dict(self) -> dict:
+        return {
+            "platform_id": self.platform_id,
+            "roms_found": self.roms_found,
+            "roms_deleted": self.roms_deleted,
+            "errors": self.errors,
+        }
+
+
+class CleanupMissingRomsTask(Task):
+    def __init__(self):
+        super().__init__(
+            title="Cleanup missing ROMs",
+            description="Delete all ROMs flagged as missing from the filesystem from the database",
+            task_type=TaskType.CLEANUP,
+            enabled=True,
+            manual_run=True,
+            cron_string=None,
+        )
+
+    @initialize_context()
+    async def run(self, platform_id: int | None = None) -> dict:
+        """Clean up ROMs that are flagged as missing from the filesystem."""
+        log.info(f"Starting {self.title} task...")
+
+        stats = CleanupMissingRomsStats(platform_id=platform_id)
+
+        filter_kwargs: dict[str, Any] = {"missing": True}
+        if platform_id is not None:
+            filter_kwargs["platform_ids"] = [platform_id]
+
+        missing_roms = db_rom_handler.get_roms_scalar(**filter_kwargs)
+
+        stats.update(roms_found=len(missing_roms))
+        log.info(
+            f"Found {len(missing_roms)} missing ROM(s) to clean up"
+            + (f" for platform ID {platform_id}" if platform_id else "")
+        )
+
+        for rom in missing_roms:
+            try:
+                log.info(
+                    f"Deleting missing ROM '{rom.name or rom.fs_name}' [ID: {rom.id}] from database"
+                )
+                db_rom_handler.delete_rom(rom.id)
+
+                try:
+                    await fs_resource_handler.remove_directory(rom.fs_resources_path)
+                except FileNotFoundError:
+                    log.warning(
+                        f"Couldn't find resources to delete for '{rom.name or rom.fs_name}'"
+                    )
+
+                stats.update(roms_deleted=stats.roms_deleted + 1)
+            except Exception as e:
+                log.error(f"Failed to delete missing ROM {rom.id}: {e}")
+                stats.update(errors=stats.errors + 1)
+
+        log.info(
+            f"Cleanup of missing ROMs completed: {stats.roms_deleted} deleted, {stats.errors} error(s)"
+        )
+        return stats.to_dict()
+
+
+cleanup_missing_roms_task = CleanupMissingRomsTask()
diff --git a/frontend/src/components/Settings/LibraryManagement/Config/MissingGames.vue b/frontend/src/components/Settings/LibraryManagement/Config/MissingGames.vue
index cb1be5196..900493026 100644
--- a/frontend/src/components/Settings/LibraryManagement/Config/MissingGames.vue
+++ b/frontend/src/components/Settings/LibraryManagement/Config/MissingGames.vue
@@ -14,6 +14,7 @@ import storeGalleryFilter from "@/stores/galleryFilter";
 import storeGalleryView from "@/stores/galleryView";
 import storePlatforms from "@/stores/platforms";
 import storeRoms from "@/stores/roms";
+import romApi from "@/services/api/rom";
 import type { Events } from "@/types/emitter";
 
 const { t } = useI18n();
@@ -26,6 +27,7 @@ const { selectedPlatform } = storeToRefs(galleryFilterStore);
 const platformsStore = storePlatforms();
 const emitter = inject<Emitter<Events>>("emitter");
 const loading = ref(false);
+const cleaningUp = ref(false);
 let timeout: ReturnType<typeof setTimeout> = setTimeout(() => {}, 400);
 
 const allPlatforms = computed(() =>
@@ -87,39 +89,31 @@ async function fetchRoms() {
     });
 }
 
-function cleanupAll() {
-  romsStore.setLimit(10000);
-  galleryFilterStore.setFilterMissing(true);
-  romsStore
-    .fetchRoms()
-    .then(() => {
-      emitter?.emit("showLoadingDialog", {
-        loading: false,
-        scrim: false,
-      });
-      if (filteredRoms.value.length > 0) {
-        emitter?.emit("showDeleteRomDialog", filteredRoms.value);
-      } else {
-        emitter?.emit("snackbarShow", {
-          msg: t("settings.no-missing-roms-to-delete"),
-          icon: "mdi-close-circle",
-          color: "red",
-          timeout: 4000,
-        });
-      }
-    })
-    .catch((error) => {
-      console.error("Error fetching missing games:", error);
-      emitter?.emit("snackbarShow", {
-        msg: t("settings.couldnt-fetch-missing-roms", { error }),
-        icon: "mdi-close-circle",
-        color: "red",
-        timeout: 4000,
-      });
-    })
-    .finally(() => {
-      galleryFilterStore.setFilterMissing(false);
+async function cleanupAll() {
+  if (cleaningUp.value) return;
+
+  cleaningUp.value = true;
+  try {
+    await romApi.cleanupMissingRoms({
+      platformId: selectedPlatform.value?.id,
     });
+    emitter?.emit("snackbarShow", {
+      msg: t("settings.cleanup-all-queued"),
+      icon: "mdi-check-circle",
+      color: "green",
+      timeout: 5000,
+    });
+  } catch (error) {
+    console.error("Error queuing cleanup task:", error);
+    emitter?.emit("snackbarShow", {
+      msg: t("settings.cleanup-all-error", { error }),
+      icon: "mdi-close-circle",
+      color: "red",
+      timeout: 4000,
+    });
+  } finally {
+    cleaningUp.value = false;
+  }
 }
 
 function resetMissingRoms() {
@@ -231,6 +225,7 @@ onUnmounted(() => {
             size="large"
             class="text-romm-red bg-toplayer"
             variant="flat"
+            :loading="cleaningUp"
             @click="cleanupAll"
           >
             {{ t("settings.cleanup-all") }}
diff --git a/frontend/src/locales/en_US/settings.json b/frontend/src/locales/en_US/settings.json
index 08c1d5b0e..ad4127db2 100644
--- a/frontend/src/locales/en_US/settings.json
+++ b/frontend/src/locales/en_US/settings.json
@@ -15,6 +15,8 @@
   "canceled": "Canceled",
   "cleanup": "Cleanup",
   "cleanup-all": "Clean up all",
+  "cleanup-all-error": "Couldn't queue cleanup task: {error}",
+  "cleanup-all-queued": "Cleanup task queued. Missing ROMs will be deleted in the background.",
   "completed": "Completed",
   "config-file-not-mounted-desc": "The config.yml file has not been mounted. Any changes made to the configuration will not persist after the application restarts.",
   "config-file-not-mounted-title": "Configuration file not mounted!",
diff --git a/frontend/src/services/api/rom.ts b/frontend/src/services/api/rom.ts
index 626268b40..0f642699b 100644
--- a/frontend/src/services/api/rom.ts
+++ b/frontend/src/services/api/rom.ts
@@ -571,6 +571,18 @@ async function deleteRoms({
   return api.post<BulkOperationResponse>("/roms/delete", payload);
 }
 
+async function cleanupMissingRoms({
+  platformId,
+}: {
+  platformId?: number | null;
+} = {}) {
+  const payload = platformId ? { platform_id: platformId } : {};
+  return api.post<{ task_id: string; status: string }>(
+    "/roms/cleanup-missing",
+    payload,
+  );
+}
+
 // Multi-note management functions
 async function createRomNote({
   romId,
@@ -653,6 +665,7 @@ export default {
   removeManual,
   updateUserRomProps,
   deleteRoms,
+  cleanupMissingRoms,
   createRomNote,
   updateRomNote,
   deleteRomNote,