diff --git a/crates/goose-cli/src/cli_prompt.rs b/crates/goose-cli/src/cli_prompt.rs
new file mode 100644
index 0000000000..9c0db7bc1a
--- /dev/null
+++ b/crates/goose-cli/src/cli_prompt.rs
@@ -0,0 +1,16 @@
+/// Returns a system prompt extension that explains CLI-specific functionality
+pub fn get_cli_prompt() -> String {
+    String::from(
+        "You are being accessed through a command-line interface. The following slash commands are available
+- you can let the user know about them if they need help:
+
+- /exit or /quit - Exit the session
+- /t - Toggle between Light/Dark/Ansi themes
+- /? or /help - Display help message
+
+Additional keyboard shortcuts:
+- Ctrl+C - Interrupt the current interaction (resets to before the interrupted request)
+- Ctrl+J - Add a newline
+- Up/Down arrows - Navigate command history"
+    )
+}
diff --git a/crates/goose-cli/src/commands/session.rs b/crates/goose-cli/src/commands/session.rs
index 0273260a68..0fb07028d2 100644
--- a/crates/goose-cli/src/commands/session.rs
+++ b/crates/goose-cli/src/commands/session.rs
@@ -161,6 +161,11 @@ pub async fn build_session(
 
     let prompt = Box::new(RustylinePrompt::new());
 
+    // Add CLI-specific system prompt extension
+    agent
+        .extend_system_prompt(crate::cli_prompt::get_cli_prompt())
+        .await;
+
     display_session_info(resume, &provider_name, &model, &session_file);
     Session::new(agent, prompt, session_file)
 }
diff --git a/crates/goose-cli/src/main.rs b/crates/goose-cli/src/main.rs
index bfe4697777..8af76d9190 100644
--- a/crates/goose-cli/src/main.rs
+++ b/crates/goose-cli/src/main.rs
@@ -9,6 +9,7 @@ pub static APP_STRATEGY: Lazy<AppStrategyArgs> = Lazy::new(|| AppStrategyArgs {
     app_name: "goose".to_string(),
 });
 
+mod cli_prompt;
 mod commands;
 mod log_usage;
 mod logging;
diff --git a/crates/goose-server/src/routes/agent.rs b/crates/goose-server/src/routes/agent.rs
index dfd683075e..46bdb1bd4e 100644
--- a/crates/goose-server/src/routes/agent.rs
+++ b/crates/goose-server/src/routes/agent.rs
@@ -17,6 +17,16 @@ struct VersionsResponse {
     default_version: String,
 }
 
+#[derive(Deserialize)]
+struct ExtendPromptRequest {
+    extension: String,
+}
+
+#[derive(Serialize)]
+struct ExtendPromptResponse {
+    success: bool,
+}
+
 #[derive(Deserialize)]
 struct CreateAgentRequest {
     version: Option<String>,
@@ -61,6 +71,30 @@ async fn get_versions() -> Json<VersionsResponse> {
     })
 }
 
+async fn extend_prompt(
+    State(state): State<AppState>,
+    headers: HeaderMap,
+    Json(payload): Json<ExtendPromptRequest>,
+) -> Result<Json<ExtendPromptResponse>, StatusCode> {
+    // Verify secret key
+    let secret_key = headers
+        .get("X-Secret-Key")
+        .and_then(|value| value.to_str().ok())
+        .ok_or(StatusCode::UNAUTHORIZED)?;
+
+    if secret_key != state.secret_key {
+        return Err(StatusCode::UNAUTHORIZED);
+    }
+
+    let mut agent = state.agent.lock().await;
+    if let Some(ref mut agent) = *agent {
+        agent.extend_system_prompt(payload.extension).await;
+        Ok(Json(ExtendPromptResponse { success: true }))
+    } else {
+        Err(StatusCode::NOT_FOUND)
+    }
+}
+
 async fn create_agent(
     State(state): State<AppState>,
     headers: HeaderMap,
@@ -132,6 +166,7 @@ pub fn routes(state: AppState) -> Router {
     Router::new()
         .route("/agent/versions", get(get_versions))
         .route("/agent/providers", get(list_providers))
+        .route("/agent/prompt", post(extend_prompt))
         .route("/agent", post(create_agent))
         .with_state(state)
 }
diff --git a/crates/goose/src/agents/agent.rs b/crates/goose/src/agents/agent.rs
index 6a595ffb69..ca681de4dc 100644
--- a/crates/goose/src/agents/agent.rs
+++ b/crates/goose/src/agents/agent.rs
@@ -28,4 +28,7 @@ pub trait Agent: Send + Sync {
 
     /// Get the total usage of the agent
     async fn usage(&self) -> Vec<ProviderUsage>;
+
+    /// Add custom text to be included in the system prompt
+    async fn extend_system_prompt(&mut self, extension: String);
 }
diff --git a/crates/goose/src/agents/capabilities.rs b/crates/goose/src/agents/capabilities.rs
index 7fcd6d20ea..e9a8764681 100644
--- a/crates/goose/src/agents/capabilities.rs
+++ b/crates/goose/src/agents/capabilities.rs
@@ -30,6 +30,7 @@ pub struct Capabilities {
     resource_capable_extensions: HashSet<String>,
     provider: Box<dyn Provider>,
     provider_usage: Mutex<Vec<ProviderUsage>>,
+    system_prompt_extensions: Vec<String>,
 }
 
 /// A flattened representation of a resource used by the agent to prepare inference
@@ -88,6 +89,7 @@ impl Capabilities {
             resource_capable_extensions: HashSet::new(),
             provider,
             provider_usage: Mutex::new(Vec::new()),
+            system_prompt_extensions: Vec::new(),
         }
     }
 
@@ -164,6 +166,11 @@ impl Capabilities {
         Ok(())
     }
 
+    /// Add a system prompt extension
+    pub fn add_system_prompt_extension(&mut self, extension: String) {
+        self.system_prompt_extensions.push(extension);
+    }
+
     /// Get a reference to the provider
     pub fn provider(&self) -> &dyn Provider {
         &*self.provider
@@ -303,7 +310,17 @@ impl Capabilities {
         context.insert("extensions", serde_json::to_value(extensions_info).unwrap());
         context.insert("current_date_time", Value::String(current_date_time));
 
-        load_prompt_file("system.md", &context).expect("Prompt should render")
+        let base_prompt = load_prompt_file("system.md", &context).expect("Prompt should render");
+
+        if self.system_prompt_extensions.is_empty() {
+            base_prompt
+        } else {
+            format!(
+                "{}\n\n# Additional Instructions:\n\n{}",
+                base_prompt,
+                self.system_prompt_extensions.join("\n\n")
+            )
+        }
     }
 
     /// Find and return a reference to the appropriate client for a tool call
diff --git a/crates/goose/src/agents/reference.rs b/crates/goose/src/agents/reference.rs
index 5d4cf86bb2..0cb2f67e9b 100644
--- a/crates/goose/src/agents/reference.rs
+++ b/crates/goose/src/agents/reference.rs
@@ -184,6 +184,11 @@ impl Agent for ReferenceAgent {
         let capabilities = self.capabilities.lock().await;
         capabilities.get_usage().await
     }
+
+    async fn extend_system_prompt(&mut self, extension: String) {
+        let mut capabilities = self.capabilities.lock().await;
+        capabilities.add_system_prompt_extension(extension);
+    }
 }
 
 register_agent!("reference", ReferenceAgent);
diff --git a/crates/goose/src/agents/truncate.rs b/crates/goose/src/agents/truncate.rs
index 5f80325dc4..d6df60cb72 100644
--- a/crates/goose/src/agents/truncate.rs
+++ b/crates/goose/src/agents/truncate.rs
@@ -292,6 +292,11 @@ impl Agent for TruncateAgent {
         let capabilities = self.capabilities.lock().await;
         capabilities.get_usage().await
     }
+
+    async fn extend_system_prompt(&mut self, extension: String) {
+        let mut capabilities = self.capabilities.lock().await;
+        capabilities.add_system_prompt_extension(extension);
+    }
 }
 
 register_agent!("truncate", TruncateAgent);