diff --git a/packages/cli/src/ui/commands/directoryCommand.test.tsx b/packages/cli/src/ui/commands/directoryCommand.test.tsx
index 40bf24cbe4..1c43149440 100644
--- a/packages/cli/src/ui/commands/directoryCommand.test.tsx
+++ b/packages/cli/src/ui/commands/directoryCommand.test.tsx
@@ -4,10 +4,13 @@
  * SPDX-License-Identifier: Apache-2.0
  */
 
-import { vi, describe, it, expect, beforeEach } from 'vitest';
+import { vi, describe, it, expect, beforeEach, afterEach } from 'vitest';
 import type { Mock } from 'vitest';
 import { directoryCommand } from './directoryCommand.js';
-import { expandHomeDir } from '../utils/directoryUtils.js';
+import {
+  expandHomeDir,
+  getDirectorySuggestions,
+} from '../utils/directoryUtils.js';
 import type { Config, WorkspaceContext } from '@google/gemini-cli-core';
 import type { MultiFolderTrustDialogProps } from '../components/MultiFolderTrustDialog.js';
 import type { CommandContext, OpenCustomDialogActionReturn } from './types.js';
@@ -17,6 +20,15 @@ import * as path from 'node:path';
 import * as trustedFolders from '../../config/trustedFolders.js';
 import type { LoadedTrustedFolders } from '../../config/trustedFolders.js';
 
+vi.mock('../utils/directoryUtils.js', async (importOriginal) => {
+  const actual =
+    await importOriginal<typeof import('../utils/directoryUtils.js')>();
+  return {
+    ...actual,
+    getDirectorySuggestions: vi.fn(),
+  };
+});
+
 describe('directoryCommand', () => {
   let mockContext: CommandContext;
   let mockConfig: Config;
@@ -217,6 +229,47 @@ describe('directoryCommand', () => {
         expect.any(Number),
       );
     });
+
+    describe('completion', () => {
+      const completion = addCommand!.completion!;
+
+      it('should return empty suggestions for an empty path', async () => {
+        const results = await completion(mockContext, '');
+        expect(results).toEqual([]);
+      });
+
+      it('should return empty suggestions for whitespace only path', async () => {
+        const results = await completion(mockContext, '  ');
+        expect(results).toEqual([]);
+      });
+
+      it('should return suggestions for a single path', async () => {
+        vi.mocked(getDirectorySuggestions).mockResolvedValue(['docs/', 'src/']);
+
+        const results = await completion(mockContext, 'd');
+
+        expect(getDirectorySuggestions).toHaveBeenCalledWith('d');
+        expect(results).toEqual(['docs/', 'src/']);
+      });
+
+      it('should return suggestions for multiple paths', async () => {
+        vi.mocked(getDirectorySuggestions).mockResolvedValue(['src/']);
+
+        const results = await completion(mockContext, 'docs/,s');
+
+        expect(getDirectorySuggestions).toHaveBeenCalledWith('s');
+        expect(results).toEqual(['docs/,src/']);
+      });
+
+      it('should handle leading whitespace in suggestions', async () => {
+        vi.mocked(getDirectorySuggestions).mockResolvedValue(['src/']);
+
+        const results = await completion(mockContext, 'docs/, s');
+
+        expect(getDirectorySuggestions).toHaveBeenCalledWith('s');
+        expect(results).toEqual(['docs/, src/']);
+      });
+    });
   });
 
   describe('add with folder trust enabled', () => {
diff --git a/packages/cli/src/ui/commands/directoryCommand.tsx b/packages/cli/src/ui/commands/directoryCommand.tsx
index f1aa62b800..872945ecea 100644
--- a/packages/cli/src/ui/commands/directoryCommand.tsx
+++ b/packages/cli/src/ui/commands/directoryCommand.tsx
@@ -14,7 +14,10 @@ import type { SlashCommand, CommandContext } from './types.js';
 import { CommandKind } from './types.js';
 import { MessageType, type HistoryItem } from '../types.js';
 import { refreshServerHierarchicalMemory } from '@google/gemini-cli-core';
-import { expandHomeDir } from '../utils/directoryUtils.js';
+import {
+  expandHomeDir,
+  getDirectorySuggestions,
+} from '../utils/directoryUtils.js';
 import type { Config } from '@google/gemini-cli-core';
 
 async function finishAddingDirectories(
@@ -80,6 +83,27 @@ export const directoryCommand: SlashCommand = {
         'Add directories to the workspace. Use comma to separate multiple paths',
       kind: CommandKind.BUILT_IN,
       autoExecute: false,
+      showCompletionLoading: false,
+      completion: async (context: CommandContext, partialArg: string) => {
+        // Support multiple paths separated by commas
+        const parts = partialArg.split(',');
+        const lastPart = parts[parts.length - 1];
+        const leadingWhitespace = lastPart.match(/^\s*/)?.[0] ?? '';
+        const trimmedLastPart = lastPart.trimStart();
+
+        if (trimmedLastPart === '') {
+          return [];
+        }
+
+        const suggestions = await getDirectorySuggestions(trimmedLastPart);
+
+        if (parts.length > 1) {
+          const prefix = parts.slice(0, -1).join(',') + ',';
+          return suggestions.map((s) => prefix + leadingWhitespace + s);
+        }
+
+        return suggestions.map((s) => leadingWhitespace + s);
+      },
       action: async (context: CommandContext, args: string) => {
         const {
           ui: { addItem },
diff --git a/packages/cli/src/ui/commands/types.ts b/packages/cli/src/ui/commands/types.ts
index 6f00695dc4..2165ab377a 100644
--- a/packages/cli/src/ui/commands/types.ts
+++ b/packages/cli/src/ui/commands/types.ts
@@ -201,5 +201,11 @@ export interface SlashCommand {
     partialArg: string,
   ) => Promise<string[]> | string[];
 
+  /**
+   * Whether to show the loading indicator while fetching completions.
+   * Defaults to true. Set to false for fast completions to avoid flicker.
+   */
+  showCompletionLoading?: boolean;
+
   subCommands?: SlashCommand[];
 }
diff --git a/packages/cli/src/ui/hooks/useSlashCompletion.ts b/packages/cli/src/ui/hooks/useSlashCompletion.ts
index 5e6631f453..7809d6cf0f 100644
--- a/packages/cli/src/ui/hooks/useSlashCompletion.ts
+++ b/packages/cli/src/ui/hooks/useSlashCompletion.ts
@@ -212,7 +212,10 @@ function useCommandSuggestions(
           return;
         }
 
-        setIsLoading(true);
+        const showLoading = leafCommand.showCompletionLoading !== false;
+        if (showLoading) {
+          setIsLoading(true);
+        }
         try {
           const rawParts = [...commandPathParts];
           if (partial) rawParts.push(partial);
diff --git a/packages/cli/src/ui/utils/directoryUtils.test.ts b/packages/cli/src/ui/utils/directoryUtils.test.ts
index e86c44d1fa..b001ece22c 100644
--- a/packages/cli/src/ui/utils/directoryUtils.test.ts
+++ b/packages/cli/src/ui/utils/directoryUtils.test.ts
@@ -4,10 +4,12 @@
  * SPDX-License-Identifier: Apache-2.0
  */
 
-import { vi, describe, it, expect } from 'vitest';
-import { expandHomeDir } from './directoryUtils.js';
+import { vi, describe, it, expect, beforeEach } from 'vitest';
+import { expandHomeDir, getDirectorySuggestions } from './directoryUtils.js';
 import type * as osActual from 'node:os';
 import * as path from 'node:path';
+import * as fs from 'node:fs';
+import * as fsPromises from 'node:fs/promises';
 
 vi.mock('@google/gemini-cli-core', async (importOriginal) => {
   const original =
@@ -33,7 +35,47 @@ vi.mock('node:os', async (importOriginal) => {
   };
 });
 
+vi.mock('node:fs', () => ({
+  existsSync: vi.fn(),
+  statSync: vi.fn(),
+}));
+
+vi.mock('node:fs/promises', () => ({
+  opendir: vi.fn(),
+}));
+
+interface MockDirent {
+  name: string;
+  isDirectory: () => boolean;
+}
+
+function createMockDir(entries: MockDirent[]) {
+  let index = 0;
+  const iterator = {
+    async next() {
+      if (index < entries.length) {
+        return { value: entries[index++], done: false };
+      }
+      return { value: undefined, done: true };
+    },
+    [Symbol.asyncIterator]() {
+      return this;
+    },
+  };
+
+  return {
+    [Symbol.asyncIterator]() {
+      return iterator;
+    },
+    close: vi.fn().mockResolvedValue(undefined),
+  };
+}
+
 describe('directoryUtils', () => {
+  beforeEach(() => {
+    vi.clearAllMocks();
+  });
+
   describe('expandHomeDir', () => {
     it('should expand ~ to the home directory', () => {
       expect(expandHomeDir('~')).toBe(mockHomeDir);
@@ -60,4 +102,216 @@ describe('directoryUtils', () => {
       expect(expandHomeDir('')).toBe('');
     });
   });
+
+  describe('getDirectorySuggestions', () => {
+    it('should return suggestions for an empty path', async () => {
+      vi.mocked(fs.existsSync).mockReturnValue(true);
+      vi.mocked(fs.statSync).mockReturnValue({
+        isDirectory: () => true,
+      } as fs.Stats);
+      vi.mocked(fsPromises.opendir).mockResolvedValue(
+        createMockDir([
+          { name: 'docs', isDirectory: () => true },
+          { name: 'src', isDirectory: () => true },
+          { name: 'file.txt', isDirectory: () => false },
+        ]) as unknown as fs.Dir,
+      );
+
+      const suggestions = await getDirectorySuggestions('');
+      expect(suggestions).toEqual([`docs${path.sep}`, `src${path.sep}`]);
+    });
+
+    it('should return suggestions for a partial path', async () => {
+      vi.mocked(fs.existsSync).mockReturnValue(true);
+      vi.mocked(fs.statSync).mockReturnValue({
+        isDirectory: () => true,
+      } as fs.Stats);
+      vi.mocked(fsPromises.opendir).mockResolvedValue(
+        createMockDir([
+          { name: 'docs', isDirectory: () => true },
+          { name: 'src', isDirectory: () => true },
+        ]) as unknown as fs.Dir,
+      );
+
+      const suggestions = await getDirectorySuggestions('d');
+      expect(suggestions).toEqual([`docs${path.sep}`]);
+    });
+
+    it('should return suggestions for a path with trailing slash', async () => {
+      vi.mocked(fs.existsSync).mockReturnValue(true);
+      vi.mocked(fs.statSync).mockReturnValue({
+        isDirectory: () => true,
+      } as fs.Stats);
+      vi.mocked(fsPromises.opendir).mockResolvedValue(
+        createMockDir([
+          { name: 'sub', isDirectory: () => true },
+        ]) as unknown as fs.Dir,
+      );
+
+      const suggestions = await getDirectorySuggestions('docs/');
+      expect(suggestions).toEqual(['docs/sub/']);
+    });
+
+    it('should return suggestions for a path with ~', async () => {
+      vi.mocked(fs.existsSync).mockReturnValue(true);
+      vi.mocked(fs.statSync).mockReturnValue({
+        isDirectory: () => true,
+      } as fs.Stats);
+      vi.mocked(fsPromises.opendir).mockResolvedValue(
+        createMockDir([
+          { name: 'Downloads', isDirectory: () => true },
+        ]) as unknown as fs.Dir,
+      );
+
+      const suggestions = await getDirectorySuggestions('~/');
+      expect(suggestions).toEqual(['~/Downloads/']);
+    });
+
+    it('should return suggestions for a partial path with ~', async () => {
+      vi.mocked(fs.existsSync).mockReturnValue(true);
+      vi.mocked(fs.statSync).mockReturnValue({
+        isDirectory: () => true,
+      } as fs.Stats);
+      vi.mocked(fsPromises.opendir).mockResolvedValue(
+        createMockDir([
+          { name: 'Downloads', isDirectory: () => true },
+        ]) as unknown as fs.Dir,
+      );
+
+      const suggestions = await getDirectorySuggestions('~/Down');
+      expect(suggestions).toEqual(['~/Downloads/']);
+    });
+
+    it('should return suggestions for ../', async () => {
+      vi.mocked(fs.existsSync).mockReturnValue(true);
+      vi.mocked(fs.statSync).mockReturnValue({
+        isDirectory: () => true,
+      } as fs.Stats);
+      vi.mocked(fsPromises.opendir).mockResolvedValue(
+        createMockDir([
+          { name: 'other-project', isDirectory: () => true },
+        ]) as unknown as fs.Dir,
+      );
+
+      const suggestions = await getDirectorySuggestions('../');
+      expect(suggestions).toEqual(['../other-project/']);
+    });
+
+    it('should ignore hidden directories', async () => {
+      vi.mocked(fs.existsSync).mockReturnValue(true);
+      vi.mocked(fs.statSync).mockReturnValue({
+        isDirectory: () => true,
+      } as fs.Stats);
+      vi.mocked(fsPromises.opendir).mockResolvedValue(
+        createMockDir([
+          { name: '.git', isDirectory: () => true },
+          { name: 'src', isDirectory: () => true },
+        ]) as unknown as fs.Dir,
+      );
+
+      const suggestions = await getDirectorySuggestions('');
+      expect(suggestions).toEqual([`src${path.sep}`]);
+    });
+
+    it('should show hidden directories when filter starts with .', async () => {
+      vi.mocked(fs.existsSync).mockReturnValue(true);
+      vi.mocked(fs.statSync).mockReturnValue({
+        isDirectory: () => true,
+      } as fs.Stats);
+      vi.mocked(fsPromises.opendir).mockResolvedValue(
+        createMockDir([
+          { name: '.git', isDirectory: () => true },
+          { name: '.github', isDirectory: () => true },
+          { name: '.vscode', isDirectory: () => true },
+          { name: 'src', isDirectory: () => true },
+        ]) as unknown as fs.Dir,
+      );
+
+      const suggestions = await getDirectorySuggestions('.g');
+      expect(suggestions).toEqual([`.git${path.sep}`, `.github${path.sep}`]);
+    });
+
+    it('should return empty array if directory does not exist', async () => {
+      vi.mocked(fs.existsSync).mockReturnValue(false);
+      const suggestions = await getDirectorySuggestions('nonexistent/');
+      expect(suggestions).toEqual([]);
+    });
+
+    it('should limit results to 50 suggestions', async () => {
+      vi.mocked(fs.existsSync).mockReturnValue(true);
+      vi.mocked(fs.statSync).mockReturnValue({
+        isDirectory: () => true,
+      } as fs.Stats);
+
+      // Create 200 directories
+      const manyDirs = Array.from({ length: 200 }, (_, i) => ({
+        name: `dir${String(i).padStart(3, '0')}`,
+        isDirectory: () => true,
+      }));
+
+      vi.mocked(fsPromises.opendir).mockResolvedValue(
+        createMockDir(manyDirs) as unknown as fs.Dir,
+      );
+
+      const suggestions = await getDirectorySuggestions('');
+      expect(suggestions).toHaveLength(50);
+    });
+
+    it('should terminate early after 150 matches for performance', async () => {
+      vi.mocked(fs.existsSync).mockReturnValue(true);
+      vi.mocked(fs.statSync).mockReturnValue({
+        isDirectory: () => true,
+      } as fs.Stats);
+
+      // Create 200 directories
+      const manyDirs = Array.from({ length: 200 }, (_, i) => ({
+        name: `dir${String(i).padStart(3, '0')}`,
+        isDirectory: () => true,
+      }));
+
+      const mockDir = createMockDir(manyDirs);
+      vi.mocked(fsPromises.opendir).mockResolvedValue(
+        mockDir as unknown as fs.Dir,
+      );
+
+      await getDirectorySuggestions('');
+
+      // The close method should be called, indicating early termination
+      expect(mockDir.close).toHaveBeenCalled();
+    });
+  });
+
+  describe.skipIf(process.platform !== 'win32')(
+    'getDirectorySuggestions (Windows)',
+    () => {
+      it('should handle %userprofile% expansion', async () => {
+        vi.mocked(fs.existsSync).mockReturnValue(true);
+        vi.mocked(fs.statSync).mockReturnValue({
+          isDirectory: () => true,
+        } as fs.Stats);
+        vi.mocked(fsPromises.opendir).mockResolvedValue(
+          createMockDir([
+            { name: 'Documents', isDirectory: () => true },
+            { name: 'Downloads', isDirectory: () => true },
+          ]) as unknown as fs.Dir,
+        );
+
+        expect(await getDirectorySuggestions('%userprofile%\\')).toEqual([
+          `%userprofile%\\Documents${path.sep}`,
+          `%userprofile%\\Downloads${path.sep}`,
+        ]);
+
+        vi.mocked(fsPromises.opendir).mockResolvedValue(
+          createMockDir([
+            { name: 'Documents', isDirectory: () => true },
+            { name: 'Downloads', isDirectory: () => true },
+          ]) as unknown as fs.Dir,
+        );
+
+        expect(await getDirectorySuggestions('%userprofile%\\Doc')).toEqual([
+          `%userprofile%\\Documents${path.sep}`,
+        ]);
+      });
+    },
+  );
 });
diff --git a/packages/cli/src/ui/utils/directoryUtils.ts b/packages/cli/src/ui/utils/directoryUtils.ts
index e389042c7c..084052525b 100644
--- a/packages/cli/src/ui/utils/directoryUtils.ts
+++ b/packages/cli/src/ui/utils/directoryUtils.ts
@@ -6,6 +6,11 @@
 
 import * as os from 'node:os';
 import * as path from 'node:path';
+import * as fs from 'node:fs';
+import { opendir } from 'node:fs/promises';
+
+const MAX_SUGGESTIONS = 50;
+const MATCH_BUFFER_MULTIPLIER = 3;
 
 export function expandHomeDir(p: string): string {
   if (!p) {
@@ -19,3 +24,118 @@ export function expandHomeDir(p: string): string {
   }
   return path.normalize(expandedPath);
 }
+
+interface ParsedPath {
+  searchDir: string;
+  filter: string;
+  isHomeExpansion: boolean;
+  resultPrefix: string;
+}
+
+function parsePartialPath(partialPath: string): ParsedPath {
+  const isHomeExpansion = partialPath.startsWith('~');
+  const expandedPath = expandHomeDir(partialPath || '.');
+
+  let searchDir: string;
+  let filter: string;
+
+  if (
+    partialPath === '' ||
+    partialPath.endsWith('/') ||
+    partialPath.endsWith(path.sep)
+  ) {
+    searchDir = expandedPath;
+    filter = '';
+  } else {
+    searchDir = path.dirname(expandedPath);
+    filter = path.basename(expandedPath);
+
+    // Special case for ~ because path.dirname('~') can be '.'
+    if (
+      isHomeExpansion &&
+      !partialPath.includes('/') &&
+      !partialPath.includes(path.sep)
+    ) {
+      searchDir = os.homedir();
+      filter = partialPath.substring(1);
+    }
+  }
+
+  // Calculate result prefix
+  let resultPrefix = '';
+  if (
+    partialPath === '' ||
+    partialPath.endsWith('/') ||
+    partialPath.endsWith(path.sep)
+  ) {
+    resultPrefix = partialPath;
+  } else {
+    const lastSlashIndex = Math.max(
+      partialPath.lastIndexOf('/'),
+      partialPath.lastIndexOf(path.sep),
+    );
+    if (lastSlashIndex !== -1) {
+      resultPrefix = partialPath.substring(0, lastSlashIndex + 1);
+    } else if (isHomeExpansion) {
+      resultPrefix = `~${path.sep}`;
+    }
+  }
+
+  return { searchDir, filter, isHomeExpansion, resultPrefix };
+}
+
+/**
+ * Gets directory suggestions based on a partial path.
+ * Uses async iteration with fs.opendir for efficient handling of large directories.
+ *
+ * @param partialPath The partial path typed by the user.
+ * @returns A promise resolving to an array of directory path suggestions.
+ */
+export async function getDirectorySuggestions(
+  partialPath: string,
+): Promise<string[]> {
+  try {
+    const { searchDir, filter, resultPrefix } = parsePartialPath(partialPath);
+
+    if (!fs.existsSync(searchDir) || !fs.statSync(searchDir).isDirectory()) {
+      return [];
+    }
+
+    const matches: string[] = [];
+    const filterLower = filter.toLowerCase();
+    const showHidden = filter.startsWith('.');
+    const dir = await opendir(searchDir);
+
+    try {
+      for await (const entry of dir) {
+        if (!entry.isDirectory()) {
+          continue;
+        }
+        if (entry.name.startsWith('.') && !showHidden) {
+          continue;
+        }
+
+        if (entry.name.toLowerCase().startsWith(filterLower)) {
+          matches.push(entry.name);
+
+          // Early termination with buffer for sorting
+          if (matches.length >= MAX_SUGGESTIONS * MATCH_BUFFER_MULTIPLIER) {
+            break;
+          }
+        }
+      }
+    } finally {
+      await dir.close().catch(() => {});
+    }
+
+    // Use the separator style from user's input for consistency
+    const userSep = resultPrefix.includes('/') ? '/' : path.sep;
+
+    return matches
+      .sort()
+      .slice(0, MAX_SUGGESTIONS)
+      .map((name) => resultPrefix + name + userSep);
+  } catch (_) {
+    return [];
+  }
+}