diff --git a/src/extension/chatSessions/vscode-node/copilotCLICustomizationProvider.ts b/src/extension/chatSessions/vscode-node/copilotCLICustomizationProvider.ts
index 5ab233178..17bbe462c 100644
--- a/src/extension/chatSessions/vscode-node/copilotCLICustomizationProvider.ts
+++ b/src/extension/chatSessions/vscode-node/copilotCLICustomizationProvider.ts
@@ -95,26 +95,33 @@ export class CopilotCLICustomizationProvider extends Disposable implements vscod
 	 * - on-demand-instructions: files without an applyTo pattern
 	 */
 	private async getInstructionItems(token: CancellationToken): Promise<vscode.ChatSessionCustomizationItem[]> {
-		const agentInstructionUris = new Set(
-			(await this.customInstructionsService.getAgentInstructions()).map(uri => uri.toString())
-		);
+		const agentInstructionUriList = await this.customInstructionsService.getAgentInstructions();
 
 		const items: vscode.ChatSessionCustomizationItem[] = [];
+		const seenUris = new Set<string>();
+
+		// Emit agent instruction files (AGENTS.md, CLAUDE.md, copilot-instructions.md)
+		// that come from customInstructionsService but may not appear in
+		// chatPromptFileService.instructions.
+		for (const uri of agentInstructionUriList) {
+			seenUris.add(uri.toString());
+			items.push({
+				uri,
+				type: vscode.ChatSessionCustomizationType.Instructions,
+				name: basename(uri),
+				groupKey: 'agent-instructions',
+			});
+		}
 
 		for (const instruction of this.chatPromptFileService.instructions) {
 			const uri = instruction.uri;
-			const name = deriveNameFromUri(uri, INSTRUCTION_FILE_EXTENSION);
 
-			if (agentInstructionUris.has(uri.toString())) {
-				items.push({
-					uri,
-					type: vscode.ChatSessionCustomizationType.Instructions,
-					name,
-					groupKey: 'agent-instructions',
-				});
-				continue;
+			if (seenUris.has(uri.toString())) {
+				continue; // already emitted as agent instruction
 			}
 
+			const name = deriveNameFromUri(uri, INSTRUCTION_FILE_EXTENSION);
+
 			let pattern: string | undefined;
 			let description: string | undefined;
 			try {
diff --git a/src/extension/chatSessions/vscode-node/test/copilotCLICustomizationProvider.spec.ts b/src/extension/chatSessions/vscode-node/test/copilotCLICustomizationProvider.spec.ts
index f5acc4d4c..2688044d1 100644
--- a/src/extension/chatSessions/vscode-node/test/copilotCLICustomizationProvider.spec.ts
+++ b/src/extension/chatSessions/vscode-node/test/copilotCLICustomizationProvider.spec.ts
@@ -348,6 +348,22 @@ describe('CopilotCLICustomizationProvider', () => {
 			expect(instrItems[0].badge).toBeUndefined();
 		});
 
+		it('emits agent instructions not in chatPromptFileService.instructions', async () => {
+			const agentsUri = URI.file('/workspace/AGENTS.md');
+			const claudeUri = URI.file('/workspace/CLAUDE.md');
+			const copilotUri = URI.file('/workspace/.github/copilot-instructions.md');
+			// Agent instructions are NOT in chatPromptFileService.instructions —
+			// they come only from customInstructionsService.getAgentInstructions().
+			mockPromptFileService.setInstructions([]);
+			mockCustomInstructionsService.setAgentInstructionUris([agentsUri, claudeUri, copilotUri]);
+
+			const items = await provider.provideChatSessionCustomizations(undefined!);
+			const instrItems = items.filter(i => i.type === FakeChatSessionCustomizationType.Instructions);
+			expect(instrItems).toHaveLength(3);
+			expect(instrItems.every(i => i.groupKey === 'agent-instructions')).toBe(true);
+			expect(instrItems.map(i => i.name)).toEqual(['AGENTS.md', 'CLAUDE.md', 'copilot-instructions.md']);
+		});
+
 		it('uses context-instructions groupKey with badge for instructions with applyTo pattern', async () => {
 			const uri = URI.file('/workspace/.github/style.instructions.md');
 			mockPromptFileService.setInstructions([{ uri }]);