diff --git a/docs/static/openapi.json b/docs/static/openapi.json
index a3e6c0ccda..954c289578 100644
--- a/docs/static/openapi.json
+++ b/docs/static/openapi.json
@@ -876,6 +876,11 @@
                     "type": "string",
                     "nullable": true
                   },
+                  "conversation_instructions": {
+                    "type": "string",
+                    "nullable": true,
+                    "description": "Optional instructions the agent must follow throughout the conversation while addressing the user's initial task"
+                  },
                   "image_urls": {
                     "type": "array",
                     "items": {
diff --git a/openhands/agenthub/codeact_agent/prompts/additional_info.j2 b/openhands/agenthub/codeact_agent/prompts/additional_info.j2
index 46b0290888..3d08e0e657 100644
--- a/openhands/agenthub/codeact_agent/prompts/additional_info.j2
+++ b/openhands/agenthub/codeact_agent/prompts/additional_info.j2
@@ -36,4 +36,9 @@ You are have access to the following environment variables
 Today's date is {{ runtime_info.date }} (UTC).
 {% endif %}
 </RUNTIME_INFORMATION>
+{% if conversation_instructions and conversation_instructions.content -%}
+<CONVERSATION_INSTRUCTIONS>
+{{ conversation_instructions.content }}
+</CONVERSATION_INSTRUCTIONS>
+{% endif %}
 {% endif %}
diff --git a/openhands/cli/main.py b/openhands/cli/main.py
index 8ba7ef532f..7d160336da 100644
--- a/openhands/cli/main.py
+++ b/openhands/cli/main.py
@@ -105,6 +105,7 @@ async def run_session(
     settings_store: FileSettingsStore,
     current_dir: str,
     task_content: str | None = None,
+    conversation_instructions: str | None = None,
     session_name: str | None = None,
 ) -> bool:
     reload_microagents = False
@@ -248,6 +249,7 @@ async def run_session(
         sid=sid,
         selected_repository=config.sandbox.selected_repo,
         repo_directory=repo_directory,
+        conversation_instructions=conversation_instructions,
     )
 
     # Add MCP tools to the agent
diff --git a/openhands/core/main.py b/openhands/core/main.py
index e9cbc45b26..0484ce14fc 100644
--- a/openhands/core/main.py
+++ b/openhands/core/main.py
@@ -55,6 +55,7 @@ async def run_controller(
     fake_user_response_fn: FakeUserResponseFunc | None = None,
     headless_mode: bool = True,
     memory: Memory | None = None,
+    conversation_instructions: str | None = None,
 ) -> State | None:
     """Main coroutine to run the agent controller with task input flexibility.
 
@@ -126,6 +127,7 @@ async def run_controller(
             sid=sid,
             selected_repository=config.sandbox.selected_repo,
             repo_directory=repo_directory,
+            conversation_instructions=conversation_instructions,
         )
 
     # Add MCP tools to the agent
diff --git a/openhands/core/setup.py b/openhands/core/setup.py
index 08fb45bc83..be54a9b093 100644
--- a/openhands/core/setup.py
+++ b/openhands/core/setup.py
@@ -135,6 +135,7 @@ def create_memory(
     selected_repository: str | None = None,
     repo_directory: str | None = None,
     status_callback: Callable | None = None,
+    conversation_instructions: str | None = None,
 ) -> Memory:
     """Create a memory for the agent to use.
 
@@ -145,6 +146,7 @@ def create_memory(
         selected_repository: The repository to clone and start with, if any.
         repo_directory: The repository directory, if any.
         status_callback: Optional callback function to handle status updates.
+        conversation_instructions: Optional instructions that are passed to the agent
     """
     memory = Memory(
         event_stream=event_stream,
@@ -152,6 +154,8 @@ def create_memory(
         status_callback=status_callback,
     )
 
+    memory.set_conversation_instructions(conversation_instructions)
+
     if runtime:
         # sets available hosts
         memory.set_runtime_info(runtime, {})
diff --git a/openhands/events/observation/agent.py b/openhands/events/observation/agent.py
index c057efa8df..f97ea2bf43 100644
--- a/openhands/events/observation/agent.py
+++ b/openhands/events/observation/agent.py
@@ -75,6 +75,7 @@ class RecallObservation(Observation):
     additional_agent_instructions: str = ''
     date: str = ''
     custom_secrets_descriptions: dict[str, str] = field(default_factory=dict)
+    conversation_instructions: str = ''
 
     # knowledge
     microagent_knowledge: list[MicroagentKnowledge] = field(default_factory=list)
@@ -117,6 +118,7 @@ class RecallObservation(Observation):
                     f'additional_agent_instructions={self.additional_agent_instructions[:20]}...',
                     f'date={self.date}'
                     f'custom_secrets_descriptions={self.custom_secrets_descriptions}',
+                    f'conversation_instructions={self.conversation_instructions[0:20]}...'
                 ]
             )
         else:
diff --git a/openhands/memory/conversation_memory.py b/openhands/memory/conversation_memory.py
index 17e39fb759..c0de1877b1 100644
--- a/openhands/memory/conversation_memory.py
+++ b/openhands/memory/conversation_memory.py
@@ -41,7 +41,12 @@ from openhands.events.observation.error import ErrorObservation
 from openhands.events.observation.mcp import MCPObservation
 from openhands.events.observation.observation import Observation
 from openhands.events.serialization.event import truncate_content
-from openhands.utils.prompt import PromptManager, RepositoryInfo, RuntimeInfo
+from openhands.utils.prompt import (
+    ConversationInstructions,
+    PromptManager,
+    RepositoryInfo,
+    RuntimeInfo,
+)
 
 
 class ConversationMemory:
@@ -467,6 +472,13 @@ class ConversationMemory:
                         custom_secrets_descriptions=obs.custom_secrets_descriptions,
                     )
 
+                conversation_instructions = None
+
+                if obs.conversation_instructions:
+                    conversation_instructions = ConversationInstructions(
+                        content=obs.conversation_instructions
+                    )
+
                 repo_instructions = (
                     obs.repo_instructions if obs.repo_instructions else ''
                 )
@@ -476,10 +488,10 @@ class ConversationMemory:
                     repo_info.repo_name or repo_info.repo_directory
                 )
                 has_runtime_info = runtime_info is not None and (
-                    runtime_info.available_hosts
-                    or runtime_info.additional_agent_instructions
+                    runtime_info.date or runtime_info.custom_secrets_descriptions
                 )
                 has_repo_instructions = bool(repo_instructions.strip())
+                has_conversation_instructions = conversation_instructions is not None
 
                 # Filter and process microagent knowledge
                 filtered_agents = []
@@ -497,11 +509,17 @@ class ConversationMemory:
                 message_content = []
 
                 # Build the workspace context information
-                if has_repo_info or has_runtime_info or has_repo_instructions:
+                if (
+                    has_repo_info
+                    or has_runtime_info
+                    or has_repo_instructions
+                    or has_conversation_instructions
+                ):
                     formatted_workspace_text = (
                         self.prompt_manager.build_workspace_context(
                             repository_info=repo_info,
                             runtime_info=runtime_info,
+                            conversation_instructions=conversation_instructions,
                             repo_instructions=repo_instructions,
                         )
                     )
diff --git a/openhands/memory/memory.py b/openhands/memory/memory.py
index b34e263196..488dc795d6 100644
--- a/openhands/memory/memory.py
+++ b/openhands/memory/memory.py
@@ -22,7 +22,11 @@ from openhands.microagent import (
     load_microagents_from_dir,
 )
 from openhands.runtime.base import Runtime
-from openhands.utils.prompt import RepositoryInfo, RuntimeInfo
+from openhands.utils.prompt import (
+    ConversationInstructions,
+    RepositoryInfo,
+    RuntimeInfo,
+)
 
 GLOBAL_MICROAGENTS_DIR = os.path.join(
     os.path.dirname(os.path.dirname(openhands.__file__)),
@@ -65,6 +69,7 @@ class Memory:
         # Store repository / runtime info to send them to the templating later
         self.repository_info: RepositoryInfo | None = None
         self.runtime_info: RuntimeInfo | None = None
+        self.conversation_instructions: ConversationInstructions | None = None
 
         # Load global microagents (Knowledge + Repo)
         # from typically OpenHands/microagents (i.e., the PUBLIC microagents)
@@ -156,6 +161,7 @@ class Memory:
             or self.runtime_info
             or repo_instructions
             or microagent_knowledge
+            or self.conversation_instructions
         ):
             obs = RecallObservation(
                 recall_type=RecallType.WORKSPACE_CONTEXT,
@@ -180,6 +186,9 @@ class Memory:
                 custom_secrets_descriptions=self.runtime_info.custom_secrets_descriptions
                 if self.runtime_info is not None
                 else {},
+                conversation_instructions=self.conversation_instructions.content
+                if self.conversation_instructions is not None
+                else '',
             )
             return obs
         return None
@@ -290,7 +299,9 @@ class Memory:
             self.repository_info = None
 
     def set_runtime_info(
-        self, runtime: Runtime, custom_secrets_descriptions: dict[str, str]
+        self,
+        runtime: Runtime,
+        custom_secrets_descriptions: dict[str, str],
     ) -> None:
         """Store runtime info (web hosts, ports, etc.)."""
         # e.g. { '127.0.0.1': 8080 }
@@ -306,9 +317,21 @@ class Memory:
             )
         else:
             self.runtime_info = RuntimeInfo(
-                date=date, custom_secrets_descriptions=custom_secrets_descriptions
+                date=date,
+                custom_secrets_descriptions=custom_secrets_descriptions,
             )
 
+    def set_conversation_instructions(
+        self, conversation_instructions: str | None
+    ) -> None:
+        """
+        Set contextual information for conversation
+        This is information the agent may require
+        """
+        self.conversation_instructions = ConversationInstructions(
+            content=conversation_instructions or ''
+        )
+
     def send_error_message(self, message_id: str, message: str):
         """Sends an error message if the callback function was provided."""
         if self.status_callback:
diff --git a/openhands/server/routes/manage_conversations.py b/openhands/server/routes/manage_conversations.py
index 73376f21b6..6a088b141c 100644
--- a/openhands/server/routes/manage_conversations.py
+++ b/openhands/server/routes/manage_conversations.py
@@ -61,6 +61,7 @@ class InitSessionRequest(BaseModel):
     image_urls: list[str] | None = None
     replay_json: str | None = None
     suggested_task: SuggestedTask | None = None
+    conversation_instructions: str | None = None
 
     model_config = {'extra': 'forbid'}
 
@@ -82,6 +83,7 @@ async def _create_new_conversation(
     initial_user_msg: str | None,
     image_urls: list[str] | None,
     replay_json: str | None,
+    conversation_instructions: str | None = None,
     conversation_trigger: ConversationTrigger = ConversationTrigger.GUI,
     attach_convo_id: bool = False,
 ) -> AgentLoopInfo:
@@ -120,6 +122,7 @@ async def _create_new_conversation(
     session_init_args['selected_repository'] = selected_repository
     session_init_args['custom_secrets'] = custom_secrets
     session_init_args['selected_branch'] = selected_branch
+    session_init_args['conversation_instructions'] = conversation_instructions
     conversation_init_data = ConversationInitData(**session_init_args)
     logger.info('Loading conversation store')
     conversation_store = await ConversationStoreImpl.get_instance(config, user_id)
@@ -195,6 +198,7 @@ async def new_conversation(
     replay_json = data.replay_json
     suggested_task = data.suggested_task
     git_provider = data.git_provider
+    conversation_instructions = data.conversation_instructions
 
     conversation_trigger = ConversationTrigger.GUI
 
@@ -222,6 +226,7 @@ async def new_conversation(
             image_urls=image_urls,
             replay_json=replay_json,
             conversation_trigger=conversation_trigger,
+            conversation_instructions=conversation_instructions
         )
 
         return InitSessionResponse(
diff --git a/openhands/server/session/agent_session.py b/openhands/server/session/agent_session.py
index e388b9c37a..5d71977cce 100644
--- a/openhands/server/session/agent_session.py
+++ b/openhands/server/session/agent_session.py
@@ -90,6 +90,7 @@ class AgentSession:
         selected_repository: str | None = None,
         selected_branch: str | None = None,
         initial_message: MessageAction | None = None,
+        conversation_instructions: str | None = None,
         replay_json: str | None = None,
     ) -> None:
         """Starts the Agent session
@@ -144,6 +145,7 @@ class AgentSession:
             self.memory = await self._create_memory(
                 selected_repository=selected_repository,
                 repo_directory=repo_directory,
+                conversation_instructions=conversation_instructions,
                 custom_secrets_descriptions=custom_secrets_handler.get_custom_secrets_descriptions()
             )
 
@@ -415,7 +417,11 @@ class AgentSession:
         return controller
 
     async def _create_memory(
-        self, selected_repository: str | None, repo_directory: str | None, custom_secrets_descriptions: dict[str, str]
+        self, 
+        selected_repository: str | None, 
+        repo_directory: str | None, 
+        conversation_instructions: str | None,
+        custom_secrets_descriptions: dict[str, str]
     ) -> Memory:
         memory = Memory(
             event_stream=self.event_stream,
@@ -426,6 +432,7 @@ class AgentSession:
         if self.runtime:
             # sets available hosts and other runtime info
             memory.set_runtime_info(self.runtime, custom_secrets_descriptions)
+            memory.set_conversation_instructions(conversation_instructions)
 
             # loads microagents from repo/.openhands/microagents
             microagents: list[BaseMicroagent] = await call_sync_from_async(
@@ -435,7 +442,10 @@ class AgentSession:
             memory.load_user_workspace_microagents(microagents)
 
             if selected_repository and repo_directory:
-                memory.set_repository_info(selected_repository, repo_directory)
+                memory.set_repository_info(
+                    selected_repository, 
+                    repo_directory
+                )
         return memory
 
     def _maybe_restore_state(self) -> State | None:
diff --git a/openhands/server/session/conversation_init_data.py b/openhands/server/session/conversation_init_data.py
index 859c9179f3..18acbb3806 100644
--- a/openhands/server/session/conversation_init_data.py
+++ b/openhands/server/session/conversation_init_data.py
@@ -14,6 +14,7 @@ class ConversationInitData(Settings):
     selected_repository: str | None = Field(default=None)
     replay_json: str | None = Field(default=None)
     selected_branch: str | None = Field(default=None)
+    conversation_instructions: str | None = Field(default=None)
 
     model_config = {
         'arbitrary_types_allowed': True,
diff --git a/openhands/server/session/session.py b/openhands/server/session/session.py
index c5239eafe6..9a690f4e87 100644
--- a/openhands/server/session/session.py
+++ b/openhands/server/session/session.py
@@ -155,11 +155,13 @@ class Session:
         selected_repository = None
         selected_branch = None
         custom_secrets = None
+        conversation_instructions = None
         if isinstance(settings, ConversationInitData):
             git_provider_tokens = settings.git_provider_tokens
             selected_repository = settings.selected_repository
             selected_branch = settings.selected_branch
             custom_secrets = settings.custom_secrets
+            conversation_instructions = settings.conversation_instructions
 
         try:
             await self.agent_session.start(
@@ -175,6 +177,7 @@ class Session:
                 selected_repository=selected_repository,
                 selected_branch=selected_branch,
                 initial_message=initial_message,
+                conversation_instructions=conversation_instructions,
                 replay_json=replay_json,
             )
         except MicroagentValidationError as e:
diff --git a/openhands/utils/prompt.py b/openhands/utils/prompt.py
index d760419ce1..ab01db86de 100644
--- a/openhands/utils/prompt.py
+++ b/openhands/utils/prompt.py
@@ -25,6 +25,20 @@ class RepositoryInfo:
     repo_directory: str | None = None
 
 
+@dataclass
+class ConversationInstructions:
+    """
+    Optional instructions the agent must follow throughout the conversation while addressing the user's initial task
+
+    Examples include
+
+        1. Resolver instructions: you're responding to GitHub issue #1234, make sure to open a PR when you are done
+        2. Slack instructions: make sure to check whether any of the context attached is relevant to the task <context_messages>
+    """
+
+    content: str = ''
+
+
 class PromptManager:
     """
     Manages prompt templates and includes information from the user's workspace micro-agents and global micro-agents.
@@ -74,6 +88,7 @@ class PromptManager:
         self,
         repository_info: RepositoryInfo | None,
         runtime_info: RuntimeInfo | None,
+        conversation_instructions: ConversationInstructions | None,
         repo_instructions: str = '',
     ) -> str:
         """Renders the additional info template with the stored repository/runtime info."""
@@ -81,6 +96,7 @@ class PromptManager:
             repository_info=repository_info,
             repository_instructions=repo_instructions,
             runtime_info=runtime_info,
+            conversation_instructions=conversation_instructions,
         ).strip()
 
     def build_microagent_info(
diff --git a/tests/unit/test_memory.py b/tests/unit/test_memory.py
index 3589e4c142..c4897a4475 100644
--- a/tests/unit/test_memory.py
+++ b/tests/unit/test_memory.py
@@ -2,11 +2,12 @@ import asyncio
 import os
 import shutil
 import time
-from unittest.mock import MagicMock, patch
+from unittest.mock import AsyncMock, MagicMock, patch
 
 import pytest
 
 from openhands.controller.agent import Agent
+from openhands.controller.agent_controller import AgentController
 from openhands.core.config import AppConfig
 from openhands.core.main import run_controller
 from openhands.core.schema.agent import AgentState
@@ -25,8 +26,14 @@ from openhands.memory.memory import Memory
 from openhands.runtime.impl.action_execution.action_execution_client import (
     ActionExecutionClient,
 )
+from openhands.server.session.agent_session import AgentSession
 from openhands.storage.memory import InMemoryFileStore
-from openhands.utils.prompt import PromptManager, RepositoryInfo, RuntimeInfo
+from openhands.utils.prompt import (
+    ConversationInstructions,
+    PromptManager,
+    RepositoryInfo,
+    RuntimeInfo,
+)
 
 
 @pytest.fixture
@@ -76,6 +83,11 @@ def mock_agent():
     system_message._id = -1  # Set invalid ID to avoid the ID check
     agent.get_system_message.return_value = system_message
 
+    agent.config = MagicMock()
+    agent.config.enable_mcp = False
+
+    return agent
+
 
 @pytest.mark.asyncio
 async def test_memory_on_event_exception_handling(memory, event_stream, mock_agent):
@@ -443,11 +455,16 @@ def test_custom_secrets_descriptions_serialization(prompt_dir):
         repo_name='test-owner/test-repo', repo_directory='/workspace/test-repo'
     )
 
+    conversation_instructions = ConversationInstructions(
+        content='additional agent context for the task'
+    )
+
     # Build the workspace context message
     workspace_context = prompt_manager.build_workspace_context(
         repository_info=repository_info,
         runtime_info=runtime_info,
         repo_instructions='Test repository instructions',
+        conversation_instructions=conversation_instructions,
     )
 
     # Verify that the workspace context includes the custom_secrets_descriptions
@@ -456,6 +473,9 @@ def test_custom_secrets_descriptions_serialization(prompt_dir):
         assert f'$**{secret_name}**' in workspace_context
         assert secret_description in workspace_context
 
+    assert '<CONVERSATION_INSTRUCTIONS>' in workspace_context
+    assert 'additional agent context for the task' in workspace_context
+
 
 def test_serialization_deserialization_with_custom_secrets():
     """Test that RecallObservation can be serialized and deserialized with custom_secrets_descriptions."""
@@ -566,3 +586,54 @@ REPOSITORY INSTRUCTIONS: This is the second test repository.
     # Clean up
     os.remove(os.path.join(prompt_dir, 'micro', f'{repo_microagent1_name}.md'))
     os.remove(os.path.join(prompt_dir, 'micro', f'{repo_microagent2_name}.md'))
+
+
+@pytest.mark.asyncio
+async def test_conversation_instructions_plumbed_to_memory(
+    mock_agent, event_stream, file_store
+):
+    # Setup
+    session = AgentSession(
+        sid='test-session',
+        file_store=file_store,
+    )
+
+    # Create a mock runtime and set it up
+    mock_runtime = MagicMock(spec=ActionExecutionClient)
+
+    # Mock the runtime creation to set up the runtime attribute
+    async def mock_create_runtime(*args, **kwargs):
+        session.runtime = mock_runtime
+        return True
+
+    session._create_runtime = AsyncMock(side_effect=mock_create_runtime)
+
+    # Create a spy on set_initial_state
+    class SpyAgentController(AgentController):
+        set_initial_state_call_count = 0
+        test_initial_state = None
+
+        def set_initial_state(self, *args, state=None, **kwargs):
+            self.set_initial_state_call_count += 1
+            self.test_initial_state = state
+            super().set_initial_state(*args, state=state, **kwargs)
+
+    # Patch AgentController
+    with (
+        patch(
+            'openhands.server.session.agent_session.AgentController', SpyAgentController
+        ),
+    ):
+        await session.start(
+            runtime_name='test-runtime',
+            config=AppConfig(),
+            agent=mock_agent,
+            max_iterations=10,
+            conversation_instructions='instructions for conversation',
+        )
+
+        # Use the memory instance from the session, not the fixture
+        assert (
+            session.memory.conversation_instructions.content
+            == 'instructions for conversation'
+        )
diff --git a/tests/unit/test_observation_serialization.py b/tests/unit/test_observation_serialization.py
index b729a60c80..74c91e5cc9 100644
--- a/tests/unit/test_observation_serialization.py
+++ b/tests/unit/test_observation_serialization.py
@@ -248,6 +248,7 @@ def test_microagent_observation_serialization():
             'custom_secrets_descriptions': {'SECRET': 'CUSTOM'},
             'date': '04/12/1023',
             'microagent_knowledge': [],
+            'conversation_instructions': 'additional_context',
         },
     }
     serialization_deserialization(original_observation_dict, RecallObservation)
@@ -266,6 +267,7 @@ def test_microagent_observation_microagent_knowledge_serialization():
             'runtime_hosts': {},
             'additional_agent_instructions': '',
             'custom_secrets_descriptions': {},
+            'conversation_instructions': 'additional_context',
             'date': '',
             'microagent_knowledge': [
                 {
diff --git a/tests/unit/test_prompt_manager.py b/tests/unit/test_prompt_manager.py
index 7a2751c02f..17b15e1129 100644
--- a/tests/unit/test_prompt_manager.py
+++ b/tests/unit/test_prompt_manager.py
@@ -7,7 +7,12 @@ from openhands.controller.state.state import State
 from openhands.core.message import Message, TextContent
 from openhands.events.observation.agent import MicroagentKnowledge
 from openhands.microagent import BaseMicroagent
-from openhands.utils.prompt import PromptManager, RepositoryInfo, RuntimeInfo
+from openhands.utils.prompt import (
+    ConversationInstructions,
+    PromptManager,
+    RepositoryInfo,
+    RuntimeInfo,
+)
 
 
 @pytest.fixture
@@ -52,7 +57,10 @@ At the user's request, repository {{ repository_info.repo_name }} has been clone
 
     # Test building additional info
     additional_info = manager.build_workspace_context(
-        repository_info=repo_info, runtime_info=None, repo_instructions=''
+        repository_info=repo_info,
+        runtime_info=None,
+        repo_instructions='',
+        conversation_instructions=None,
     )
     assert '<REPOSITORY_INFO>' in additional_info
     assert (
@@ -205,7 +213,14 @@ each of which has a corresponding port:
 {% if runtime_info.additional_agent_instructions %}
 {{ runtime_info.additional_agent_instructions }}
 {% endif %}
+
+Today's date is {{ runtime_info.date }}
 </RUNTIME_INFORMATION>
+{% if conversation_instructions.content %}
+<CONVERSATION_INSTRUCTIONS>
+{{ conversation_instructions.content }}
+</CONVERSATION_INSTRUCTIONS>
+{% endif %}
 {% endif %}
 """)
 
@@ -221,11 +236,14 @@ each of which has a corresponding port:
     )
     repo_instructions = 'This repository contains important code.'
 
+    conversation_instructions = ConversationInstructions(content='additional context')
+
     # Build additional info
     result = manager.build_workspace_context(
         repository_info=repo_info,
         runtime_info=runtime_info,
         repo_instructions=repo_instructions,
+        conversation_instructions=conversation_instructions,
     )
 
     # Check that all information is included
@@ -237,7 +255,8 @@ each of which has a corresponding port:
     assert '<RUNTIME_INFORMATION>' in result
     assert 'example.com (port 8080)' in result
     assert 'You know everything about this runtime.' in result
-    assert "Today's date is 02/12/1232 (UTC)."
+    assert "Today's date is 02/12/1232" in result
+    assert 'additional context' in result
 
     # Clean up
     os.remove(os.path.join(prompt_dir, 'additional_info.j2'))