diff --git a/airflow-core/src/airflow/ui/openapi-gen/queries/useDagsInfinite.ts b/airflow-core/src/airflow/ui/openapi-gen/queries/useDagsInfinite.ts
new file mode 100644
index 0000000000000..2776977ce46d3
--- /dev/null
+++ b/airflow-core/src/airflow/ui/openapi-gen/queries/useDagsInfinite.ts
@@ -0,0 +1,58 @@
+/*!
+ * Licensed to the Apache Software Foundation (ASF) under one
+ * or more contributor license agreements.  See the NOTICE file
+ * distributed with this work for additional information
+ * regarding copyright ownership.  The ASF licenses this file
+ * to you under the Apache License, Version 2.0 (the
+ * "License"); you may not use this file except in compliance
+ * with the License.  You may obtain a copy of the License at
+ *
+ *   http://www.apache.org/licenses/LICENSE-2.0
+ *
+ * Unless required by applicable law or agreed to in writing,
+ * software distributed under the License is distributed on an
+ * "AS IS" BASIS, WITHOUT WARRANTIES OR CONDITIONS OF ANY
+ * KIND, either express or implied.  See the License for the
+ * specific language governing permissions and limitations
+ * under the License.
+ */
+import { InfiniteData, useInfiniteQuery, UseInfiniteQueryOptions } from "@tanstack/react-query";
+
+import { DagService } from "openapi/requests/services.gen";
+import { DAGTagCollectionResponse } from "openapi/requests/types.gen";
+
+import * as Common from "./common";
+
+export const useDagTagsInfinite = <TError = unknown, TQueryKey extends Array<unknown> = unknown[]>(
+  {
+    limit,
+    orderBy,
+    tagNamePattern,
+  }: {
+    limit?: number;
+    orderBy?: string;
+    tagNamePattern?: string;
+  } = {},
+  queryKey?: TQueryKey,
+  options?: Omit<
+    UseInfiniteQueryOptions<
+      DAGTagCollectionResponse,
+      TError,
+      InfiniteData<DAGTagCollectionResponse>,
+      DAGTagCollectionResponse,
+      unknown[],
+      number
+    >,
+    "queryKey" | "queryFn"
+  >,
+) =>
+  useInfiniteQuery({
+    queryKey: Common.UseDagServiceGetDagTagsKeyFn({ limit, orderBy, tagNamePattern }, queryKey),
+    queryFn: ({ pageParam }) => DagService.getDagTags({ limit, offset: pageParam, orderBy, tagNamePattern }),
+    initialPageParam: 0,
+    getNextPageParam: (lastPage, _allPages, lastPageParam, _allPageParams) =>
+      lastPageParam < lastPage.total_entries ? lastPage.tags.length + lastPageParam : undefined,
+    getPreviousPageParam: (firstPage, _allPages, firstPageParam, _allPageParams) =>
+      firstPageParam > 0 ? -firstPage.tags.length + firstPageParam : undefined,
+    ...options,
+  });
diff --git a/airflow-core/src/airflow/ui/src/pages/DagsList/DagsFilters.tsx b/airflow-core/src/airflow/ui/src/pages/DagsList/DagsFilters.tsx
index 8e3ac9c1b0d43..6f650c8c6972b 100644
--- a/airflow-core/src/airflow/ui/src/pages/DagsList/DagsFilters.tsx
+++ b/airflow-core/src/airflow/ui/src/pages/DagsList/DagsFilters.tsx
@@ -25,11 +25,11 @@ import {
   type SelectValueChangeDetails,
 } from "@chakra-ui/react";
 import { Select as ReactSelect, type MultiValue } from "chakra-react-select";
-import { useCallback } from "react";
+import { useCallback, useState } from "react";
 import { LuX } from "react-icons/lu";
 import { useSearchParams } from "react-router-dom";
 
-import { useDagServiceGetDagTags } from "openapi/queries";
+import { useDagTagsInfinite } from "openapi/queries/useDagsInfinite";
 import { useTableURLState } from "src/components/DataTable/useTableUrlState";
 import { QuickFilterButton } from "src/components/QuickFilterButton";
 import { StateBadge } from "src/components/StateBadge";
@@ -64,8 +64,12 @@ export const DagsFilters = () => {
   const isFailed = state === "failed";
   const isSuccess = state === "success";
 
-  const { data } = useDagServiceGetDagTags({
+  const [pattern, setPattern] = useState("");
+
+  const { data, fetchNextPage, fetchPreviousPage } = useDagTagsInfinite({
+    limit: 10,
     orderBy: "name",
+    tagNamePattern: pattern,
   });
 
   const hidePausedDagsByDefault = Boolean(useConfig("hide_paused_dags_by_default"));
@@ -132,6 +136,7 @@ export const DagsFilters = () => {
     searchParams.delete(TAGS_PARAM);
 
     setSearchParams(searchParams);
+    setPattern("");
   };
 
   let filterCount = 0;
@@ -222,11 +227,20 @@ export const DagsFilters = () => {
             isMulti
             noOptionsMessage={() => "No tags found"}
             onChange={handleSelectTagsChange}
+            onInputChange={(newValue) => setPattern(newValue)}
+            onMenuScrollToBottom={() => {
+              void fetchNextPage();
+            }}
+            onMenuScrollToTop={() => {
+              void fetchPreviousPage();
+            }}
             options={
-              data?.tags.map((tag) => ({
-                label: tag,
-                value: tag,
-              })) ?? []
+              data?.pages.flatMap((response) =>
+                response.tags.map((tag) => ({
+                  label: tag,
+                  value: tag,
+                })),
+              ) ?? []
             }
             placeholder="Filter by tag"
             value={selectedTags.map((tag) => ({