diff --git a/lib/Service/ChatService.php b/lib/Service/ChatService.php
index 1f27de531..b2be960a3 100644
--- a/lib/Service/ChatService.php
+++ b/lib/Service/ChatService.php
@@ -456,15 +456,7 @@ public function scheduleMessageGeneration(?string $userId, int $sessionId, int $
 			}
 		} else {
 			// classic chat
-			$systemPrompt = '';
-			try {
-				$firstMessage = $this->messageMapper->getFirstNMessages($sessionId, 1, Message::ROLE_SYSTEM);
-				$systemPrompt = $firstMessage->getContent();
-			} catch (DoesNotExistException $e) {
-				$this->logger->info('No system message found in the session', ['exception' => $e, 'sessionId' => $sessionId]);
-			} catch (MultipleObjectsReturnedException|Exception $e) {
-				throw new InternalException(previous: $e);
-			}
+			$systemPrompt = $this->getSessionSystemPrompt($sessionId);
 			try {
 				$history = $this->getRawLastMessages($sessionId);
 			} catch (Exception|AppConfigTypeConflictException $e) {
@@ -575,8 +567,10 @@ public function scheduleAssignmentMessageGeneration(?string $userId, int $sessio
 		$lastConversationToken = self::EMPTY_CONVERSATION_TOKEN;
 
 		// classic agency
+		// The chat user instructions are meant for interactive chats (e.g. asking for clarification),
+		// an assignment runs unattended with its own prompt
 		$prompt = $lastUserMessage->getContent();
-		$taskId = $this->scheduleAgencyTask($userId, $prompt, 0, $lastConversationToken, $sessionId);
+		$taskId = $this->scheduleAgencyTask($userId, $prompt, 0, $lastConversationToken, $sessionId, withUserInstructions: false);
 		return $taskId;
 	}
 
@@ -655,6 +649,43 @@ public function isMultimodalContextAgentAvailable(): bool {
 		return in_array(\OCP\TaskProcessing\TaskTypes\MultimodalContextAgentInteraction::ID, $this->taskProcessingManager->getAvailableTaskTypeIds());
 	}
 
+	/**
+	 * Get the user instructions stored as the system message of the session (empty string if there is none)
+	 *
+	 * @throws InternalException
+	 */
+	private function getSessionSystemPrompt(int $sessionId): string {
+		try {
+			$firstMessage = $this->messageMapper->getFirstNMessages($sessionId, 1, Message::ROLE_SYSTEM);
+			return $firstMessage->getContent();
+		} catch (DoesNotExistException $e) {
+			$this->logger->info('No system message found in the session', ['exception' => $e, 'sessionId' => $sessionId]);
+		} catch (MultipleObjectsReturnedException|Exception $e) {
+			throw new InternalException(previous: $e);
+		}
+		return '';
+	}
+
+	/**
+	 * Pass the session's user instructions to an agency task if its provider supports them.
+	 * The agent appends them to its own system prompt, they do not replace it.
+	 * If they cannot be read, the task is scheduled without them.
+	 */
+	private function addAgencyUserInstructions(array &$taskInput, array $optionalInputShape, int $sessionId): void {
+		if (!isset($optionalInputShape['user_instructions'])) {
+			return;
+		}
+		try {
+			$userInstructions = $this->getSessionSystemPrompt($sessionId);
+		} catch (InternalException $e) {
+			$this->logger->warning('Could not get the user instructions of the session, the agent will run without them', ['exception' => $e, 'sessionId' => $sessionId]);
+			return;
+		}
+		if ($userInstructions !== '') {
+			$taskInput['user_instructions'] = $userInstructions;
+		}
+	}
+
 	private function getAudioHistory(array $history): array {
 		// history is a list of JSON strings
 		// The content is the remote audio ID (or the transcription as fallback)
@@ -825,6 +856,7 @@ private function scheduleAgencyTask(
 		int $confirmation,
 		string $conversationToken,
 		int $sessionId,
+		bool $withUserInstructions = true,
 	): int {
 		$customId = 'chatty-llm:' . $sessionId;
 		$this->checkIfSessionIsThinking($userId, $customId);
@@ -834,9 +866,13 @@ private function scheduleAgencyTask(
 			'conversation_token' => $conversationToken,
 		];
 		/** @psalm-suppress UndefinedClass */
-		if (isset($this->taskProcessingManager->getAvailableTaskTypes()[\OCP\TaskProcessing\TaskTypes\ContextAgentInteraction::ID]['optionalInputShape']['memories'])) {
+		$optionalInputShape = $this->taskProcessingManager->getAvailableTaskTypes()[\OCP\TaskProcessing\TaskTypes\ContextAgentInteraction::ID]['optionalInputShape'] ?? [];
+		if (isset($optionalInputShape['memories'])) {
 			$taskInput['memories'] = $this->sessionSummaryService->getMemories($userId);
 		}
+		if ($withUserInstructions) {
+			$this->addAgencyUserInstructions($taskInput, $optionalInputShape, $sessionId);
+		}
 		/** @psalm-suppress UndefinedClass */
 		$task = new Task(
 			\OCP\TaskProcessing\TaskTypes\ContextAgentInteraction::ID,
@@ -887,6 +923,9 @@ private function scheduleAgencyMultimodalTask(
 		];
 		$taskInput['memories'] = $this->sessionSummaryService->getMemories($userId);
 		/** @psalm-suppress UndefinedClass */
+		$optionalInputShape = $this->taskProcessingManager->getAvailableTaskTypes()[\OCP\TaskProcessing\TaskTypes\MultimodalContextAgentInteraction::ID]['optionalInputShape'] ?? [];
+		$this->addAgencyUserInstructions($taskInput, $optionalInputShape, $sessionId);
+		/** @psalm-suppress UndefinedClass */
 		$task = new Task(
 			\OCP\TaskProcessing\TaskTypes\MultimodalContextAgentInteraction::ID,
 			$taskInput,
@@ -979,9 +1018,11 @@ private function scheduleAgencyAudioTask(
 			'conversation_token' => $conversationToken,
 		];
 		/** @psalm-suppress UndefinedClass */
-		if (isset($this->taskProcessingManager->getAvailableTaskTypes()[\OCP\TaskProcessing\TaskTypes\ContextAgentAudioInteraction::ID]['optionalInputShape']['memories'])) {
+		$optionalInputShape = $this->taskProcessingManager->getAvailableTaskTypes()[\OCP\TaskProcessing\TaskTypes\ContextAgentAudioInteraction::ID]['optionalInputShape'] ?? [];
+		if (isset($optionalInputShape['memories'])) {
 			$taskInput['memories'] = $this->sessionSummaryService->getMemories($userId);
 		}
+		$this->addAgencyUserInstructions($taskInput, $optionalInputShape, $sessionId);
 		/** @psalm-suppress UndefinedClass */
 		$task = new Task(
 			\OCP\TaskProcessing\TaskTypes\ContextAgentAudioInteraction::ID,
diff --git a/lib/TaskProcessing/ContextAgentAudioInteractionProvider.php b/lib/TaskProcessing/ContextAgentAudioInteractionProvider.php
index a523d72f1..d5de92831 100644
--- a/lib/TaskProcessing/ContextAgentAudioInteractionProvider.php
+++ b/lib/TaskProcessing/ContextAgentAudioInteractionProvider.php
@@ -68,6 +68,11 @@ public function getOptionalInputShape(): array {
 				$this->l->t('The memories to be injected into the chat session.'),
 				EShapeType::ListOfTexts
 			),
+			'user_instructions' => new ShapeDescriptor(
+				$this->l->t('User instructions'),
+				$this->l->t('Additional instructions for the agent, appended to its system prompt.'),
+				EShapeType::Text
+			),
 		];
 	}
 
@@ -130,10 +135,20 @@ public function process(?string $userId, array $input, callable $reportProgress)
 				'confirmation' => $confirmation,
 				'conversation_token' => $conversationToken,
 			];
+			$availableTaskTypes = $this->taskProcessingManager->getAvailableTaskTypes();
 			/** @psalm-suppress UndefinedClass */
-			if (isset($input['memories'], $this->taskProcessingManager->getAvailableTaskTypes()[ContextAgentAudioInteraction::ID]['optionalInputShape']['memories'])) {
+			if (isset($input['memories'], $availableTaskTypes[ContextAgentAudioInteraction::ID]['optionalInputShape']['memories'])) {
 				$contextAgentTaskInput['memories'] = $input['memories'];
 			}
+			/** @psalm-suppress UndefinedClass */
+			if (isset($input['user_instructions'], $availableTaskTypes[ContextAgentInteraction::ID]['optionalInputShape']['user_instructions'])) {
+				$contextAgentTaskInput['user_instructions'] = $input['user_instructions'];
+			}
+			// the reply is read out loud, so the agent must not format it (e.g. with Markdown)
+			/** @psalm-suppress UndefinedClass */
+			if (isset($availableTaskTypes[ContextAgentInteraction::ID]['optionalInputShape']['output_mode'])) {
+				$contextAgentTaskInput['output_mode'] = 'speech';
+			}
 			/** @psalm-suppress UndefinedClass,InvalidArgument */
 			$task = new Task(
 				ContextAgentInteraction::ID,
diff --git a/src/components/AdminSettings.vue b/src/components/AdminSettings.vue
index dea8caa66..6606deb3c 100644
--- a/src/components/AdminSettings.vue
+++ b/src/components/AdminSettings.vue
@@ -144,6 +144,10 @@
 					{{ t('assistant', 'It is passed on to the LLM for it to better understand the context.') }}
 					<br>
 					{{ t('assistant', '"{user}" is a placeholder for the user\'s display name.') }}
+					<template v-if="state.context_agent_available">
+						<br>
+						{{ t('assistant', 'When chatting through the Context Agent, these instructions are added to the agent\'s own instructions (requires Context Agent 2.10.0 or later).') }}
+					</template>
 				</NcNoteCard>
 				<NcRichContenteditable id="chat_user_instructions"
 					v-model="state.chat_user_instructions"
diff --git a/tests/unit/Service/ChatServiceAgencyTest.php b/tests/unit/Service/ChatServiceAgencyTest.php
new file mode 100644
index 000000000..ea5cfab99
--- /dev/null
+++ b/tests/unit/Service/ChatServiceAgencyTest.php
@@ -0,0 +1,154 @@
+<?php
+
+declare(strict_types=1);
+
+/**
+ * SPDX-FileCopyrightText: 2026 Nextcloud GmbH and Nextcloud contributors
+ * SPDX-License-Identifier: AGPL-3.0-or-later
+ */
+
+namespace OCA\Assistant\Tests\Unit\Service;
+
+use OCA\Assistant\Db\ChattyLLM\Message;
+use OCA\Assistant\Db\ChattyLLM\MessageMapper;
+use OCA\Assistant\Db\ChattyLLM\Session;
+use OCA\Assistant\Db\ChattyLLM\SessionMapper;
+use OCA\Assistant\Service\ChatService;
+use OCA\Assistant\Service\SessionSummaryService;
+use OCP\AppFramework\Db\DoesNotExistException;
+use OCP\AppFramework\Utility\ITimeFactory;
+use OCP\DB\Exception;
+use OCP\IAppConfig;
+use OCP\IDBConnection;
+use OCP\IL10N;
+use OCP\IUserManager;
+use OCP\TaskProcessing\IManager;
+use OCP\TaskProcessing\Task;
+use OCP\TaskProcessing\TaskTypes\ContextAgentInteraction;
+use PHPUnit\Framework\MockObject\MockObject;
+use Psr\Log\LoggerInterface;
+use Test\TestCase;
+
+/**
+ * Passing the Chat User Instructions to the Context Agent (nextcloud/assistant#338)
+ */
+class ChatServiceAgencyTest extends TestCase {
+
+	private const USER_ID = 'agency_test_user';
+	private const SESSION_ID = 42;
+	private const USER_INSTRUCTIONS = 'Always answer like a pirate.';
+
+	private ChatService $service;
+	private MessageMapper&MockObject $messageMapper;
+	private IManager&MockObject $taskProcessingManager;
+	private ?Task $scheduledTask = null;
+
+	protected function setUp(): void {
+		parent::setUp();
+
+		$sessionMapper = $this->createMock(SessionMapper::class);
+		$sessionMapper->method('exists')->willReturn(true);
+		$session = new Session();
+		$session->setUserId(self::USER_ID);
+		$sessionMapper->method('getUserSession')->willReturn($session);
+
+		$humanMessage = new Message();
+		$humanMessage->setSessionId(self::SESSION_ID);
+		$humanMessage->setRole(Message::ROLE_HUMAN);
+		$humanMessage->setContent('What is your name?');
+		$humanMessage->setAttachments('[]');
+		$this->messageMapper = $this->createMock(MessageMapper::class);
+		$this->messageMapper->method('getLastHumanMessage')->willReturn($humanMessage);
+
+		// only the classic Context Agent is available, no multimodal or audio agency
+		$this->taskProcessingManager = $this->createMock(IManager::class);
+		$this->taskProcessingManager->method('getAvailableTaskTypeIds')->willReturn([ContextAgentInteraction::ID]);
+		$this->taskProcessingManager->method('getUserTasksByApp')->willReturn([]);
+		$this->taskProcessingManager->method('scheduleTask')->willReturnCallback(function (Task $task): void {
+			$this->scheduledTask = $task;
+		});
+
+		$this->service = new ChatService(
+			$this->createMock(IUserManager::class),
+			$this->createMock(IAppConfig::class),
+			$this->createMock(IL10N::class),
+			$sessionMapper,
+			$this->messageMapper,
+			$this->createMock(IDBConnection::class),
+			$this->createMock(SessionSummaryService::class),
+			$this->taskProcessingManager,
+			$this->createMock(LoggerInterface::class),
+			$this->createMock(ITimeFactory::class),
+		);
+	}
+
+	private function setAgentOptionalInputs(array $optionalInputShape): void {
+		$this->taskProcessingManager->method('getAvailableTaskTypes')->willReturn([
+			ContextAgentInteraction::ID => ['optionalInputShape' => $optionalInputShape],
+		]);
+	}
+
+	private function systemMessage(string $content): Message {
+		$message = new Message();
+		$message->setSessionId(self::SESSION_ID);
+		$message->setRole(Message::ROLE_SYSTEM);
+		$message->setContent($content);
+		return $message;
+	}
+
+	public function testUserInstructionsArePassedToTheAgent(): void {
+		$this->setAgentOptionalInputs(['user_instructions' => 'shape']);
+		$this->messageMapper->method('getFirstNMessages')
+			->with(self::SESSION_ID, 1, Message::ROLE_SYSTEM)
+			->willReturn($this->systemMessage(self::USER_INSTRUCTIONS));
+
+		$this->service->scheduleMessageGeneration(self::USER_ID, self::SESSION_ID);
+
+		$this->assertNotNull($this->scheduledTask);
+		$this->assertSame(ContextAgentInteraction::ID, $this->scheduledTask->getTaskTypeId());
+		$this->assertSame(self::USER_INSTRUCTIONS, $this->scheduledTask->getInput()['user_instructions'] ?? null);
+	}
+
+	public function testUserInstructionsAreNotSentWhenTheAgentDoesNotSupportThem(): void {
+		// e.g. an older Context Agent version that does not declare the optional input
+		$this->setAgentOptionalInputs([]);
+		$this->messageMapper->expects($this->never())->method('getFirstNMessages');
+
+		$this->service->scheduleMessageGeneration(self::USER_ID, self::SESSION_ID);
+
+		$this->assertNotNull($this->scheduledTask);
+		$this->assertArrayNotHasKey('user_instructions', $this->scheduledTask->getInput());
+	}
+
+	public function testUserInstructionsAreNotSentWhenTheSessionHasNoSystemMessage(): void {
+		$this->setAgentOptionalInputs(['user_instructions' => 'shape']);
+		$this->messageMapper->method('getFirstNMessages')->willThrowException(new DoesNotExistException('no system message'));
+
+		$this->service->scheduleMessageGeneration(self::USER_ID, self::SESSION_ID);
+
+		$this->assertNotNull($this->scheduledTask);
+		$this->assertArrayNotHasKey('user_instructions', $this->scheduledTask->getInput());
+	}
+
+	public function testTheAgentRunsWithoutUserInstructionsWhenTheyCannotBeRead(): void {
+		$this->setAgentOptionalInputs(['user_instructions' => 'shape']);
+		$this->messageMapper->method('getFirstNMessages')->willThrowException(new Exception('database error'));
+
+		$this->service->scheduleMessageGeneration(self::USER_ID, self::SESSION_ID);
+
+		$this->assertNotNull($this->scheduledTask);
+		$this->assertArrayNotHasKey('user_instructions', $this->scheduledTask->getInput());
+	}
+
+	public function testUserInstructionsAreNotSentForAssignmentRuns(): void {
+		// assignments run unattended, instructions like "ask for clarification" do not apply
+		$this->setAgentOptionalInputs(['user_instructions' => 'shape']);
+		$this->messageMapper->expects($this->never())->method('getFirstNMessages');
+
+		$this->service->scheduleAssignmentMessageGeneration(self::USER_ID, self::SESSION_ID);
+
+		$this->assertNotNull($this->scheduledTask);
+		$this->assertSame(ContextAgentInteraction::ID, $this->scheduledTask->getTaskTypeId());
+		$this->assertArrayNotHasKey('user_instructions', $this->scheduledTask->getInput());
+	}
+}