diff --git a/src/search/BaseSearchSource.ts b/src/search/BaseSearchSource.ts
index d018ef0ae..d8907e546 100644
--- a/src/search/BaseSearchSource.ts
+++ b/src/search/BaseSearchSource.ts
@@ -6,6 +6,8 @@ import type {
   SearchSourceState,
   SearchSourceType,
 } from './types';
+import type { APIError } from '../errors';
+import { isAPIError, isErrorRetryable } from '../errors';
 
 export type DebounceOptions = {
   debounceMs: number;
@@ -237,6 +239,9 @@ export abstract class BaseSearchSource<T>
       stateUpdate.items = await this.filterQueryResults(items);
     } catch (e) {
       stateUpdate.lastQueryError = e as Error;
+      if (isAPIError(e as Error) && !isErrorRetryable(e as APIError)) {
+        stateUpdate.hasNext = false;
+      }
     } finally {
       this.state.next(this.getStateAfterQuery(stateUpdate, hasNewSearchQuery));
     }
@@ -285,6 +290,9 @@ export abstract class BaseSearchSourceSync<T>
       stateUpdate.items = this.filterQueryResults(items);
     } catch (e) {
       stateUpdate.lastQueryError = e as Error;
+      if (isAPIError(e as Error) && !isErrorRetryable(e as APIError)) {
+        stateUpdate.hasNext = false;
+      }
     } finally {
       this.state.next(this.getStateAfterQuery(stateUpdate, hasNewSearchQuery));
     }
diff --git a/test/unit/search/SearchController.test.js b/test/unit/search/SearchController.test.js
index d9671cdda..6d75704cf 100644
--- a/test/unit/search/SearchController.test.js
+++ b/test/unit/search/SearchController.test.js
@@ -10,7 +10,9 @@ import {
 import { generateUser } from '../test-utils/generateUser';
 import { generateChannel } from '../test-utils/generateChannel';
 
-import { describe, it, expect, beforeEach, afterEach } from 'vitest';
+import { describe, it, expect, beforeEach, afterEach, vi } from 'vitest';
+import { ErrorFromResponse } from '../../../src';
+import { APIErrorCodes } from '../../../src/errors';
 
 describe('SearchController', () => {
 	let searchController;
@@ -407,6 +409,42 @@ describe('BaseSearchSource and implementations', () => {
 				expect(searchSource.items).to.deep.equal(['item1']);
 				expect(searchSource.hasNext).to.be.false;
 			});
+
+			it('stores error from a failed request, keeps ability to paginate', async () => {
+				searchSource.pageSize = 1;
+				searchSource.state.partialNext({
+					items: [],
+					isActive: true,
+					searchQuery: 'test',
+				});
+
+				vi.spyOn(searchSource, 'query').mockRejectedValue(new Error('anything'));
+
+				await searchSource.executeQuery();
+				expect(searchSource.items).toStrictEqual([]);
+				expect(searchSource.hasNext).toBe(true);
+			});
+
+			it('terminates pagination on non-retryable error', async () => {
+				searchSource.pageSize = 1;
+				searchSource.state.partialNext({
+					items: [],
+					isActive: true,
+					searchQuery: 'test',
+				});
+
+				vi.spyOn(searchSource, 'query').mockRejectedValue(
+					new ErrorFromResponse('anything', {
+						code: APIErrorCodes[4],
+						response: {},
+						status: 400,
+					}),
+				);
+
+				await searchSource.executeQuery();
+				expect(searchSource.items).toStrictEqual([]);
+				expect(searchSource.hasNext).toBe(false);
+			});
 		});
 
 		describe('search debounce', () => {