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/DagsFilters.tsx b/airflow-core/src/airflow/ui/src/pages/DagsList/DagsFilters/DagsFilters.tsx
index d36e2b2f8ef46..195774a876822 100644
--- a/airflow-core/src/airflow/ui/src/pages/DagsList/DagsFilters/DagsFilters.tsx
+++ b/airflow-core/src/airflow/ui/src/pages/DagsList/DagsFilters/DagsFilters.tsx
@@ -18,10 +18,10 @@
  */
 import { Box, HStack } from "@chakra-ui/react";
 import type { MultiValue } from "chakra-react-select";
-import { useCallback } from "react";
+import { useCallback, useState } from "react";
 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 { SearchParamsKeys, type SearchParamsKeysType } from "src/constants/searchParams";
 import { useConfig } from "src/queries/useConfig";
@@ -66,8 +66,12 @@ 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"));
@@ -136,6 +140,7 @@ export const DagsFilters = () => {
     searchParams.delete(TAGS_MATCH_MODE_PARAM);
 
     setSearchParams(searchParams);
+    setPattern("");
   };
 
   const handleTagModeChange = useCallback(
@@ -166,11 +171,18 @@ export const DagsFilters = () => {
           showPaused={showPaused}
         />
         <TagFilter
+          onMenuScrollToBottom={() => {
+            void fetchNextPage();
+          }}
+          onMenuScrollToTop={() => {
+            void fetchPreviousPage();
+          }}
           onSelectTagsChange={handleSelectTagsChange}
           onTagModeChange={handleTagModeChange}
+          onUpdate={setPattern}
           selectedTags={selectedTags}
           tagFilterMode={tagFilterMode}
-          tags={data?.tags ?? []}
+          tags={data?.pages.flatMap((dagResponse) => dagResponse.tags) ?? []}
         />
       </HStack>
       <Box>
diff --git a/airflow-core/src/airflow/ui/src/pages/DagsList/DagsFilters/TagFilter.tsx b/airflow-core/src/airflow/ui/src/pages/DagsList/DagsFilters/TagFilter.tsx
index 57fa2b1089de1..c53429452f7cf 100644
--- a/airflow-core/src/airflow/ui/src/pages/DagsList/DagsFilters/TagFilter.tsx
+++ b/airflow-core/src/airflow/ui/src/pages/DagsList/DagsFilters/TagFilter.tsx
@@ -23,16 +23,22 @@ import { useTranslation } from "react-i18next";
 import { Switch } from "src/components/ui";
 
 type Props = {
+  readonly onMenuScrollToBottom: () => void;
+  readonly onMenuScrollToTop: () => void;
   readonly onSelectTagsChange: (tags: MultiValue<{ label: string; value: string }>) => void;
   readonly onTagModeChange: ({ checked }: { checked: boolean }) => void;
+  readonly onUpdate: (newValue: string) => void;
   readonly selectedTags: Array<string>;
   readonly tagFilterMode: string;
   readonly tags: Array<string>;
 };
 
 export const TagFilter = ({
+  onMenuScrollToBottom,
+  onMenuScrollToTop,
   onSelectTagsChange,
   onTagModeChange,
+  onUpdate,
   selectedTags,
   tagFilterMode,
   tags,
@@ -66,6 +72,9 @@ export const TagFilter = ({
           isMulti
           noOptionsMessage={() => translate("table.noTagsFound")}
           onChange={onSelectTagsChange}
+          onInputChange={(newValue) => onUpdate(newValue)}
+          onMenuScrollToBottom={onMenuScrollToBottom}
+          onMenuScrollToTop={onMenuScrollToTop}
           options={tags.map((tag) => ({
             label: tag,
             value: tag,