diff --git a/codex-rs/app-server-protocol/src/protocol.rs b/codex-rs/app-server-protocol/src/protocol.rs
index 05c9d91fb2..45562657a7 100644
--- a/codex-rs/app-server-protocol/src/protocol.rs
+++ b/codex-rs/app-server-protocol/src/protocol.rs
@@ -321,6 +321,10 @@ pub struct NewConversationParams {
     #[serde(skip_serializing_if = "Option::is_none")]
     pub base_instructions: Option<String>,
 
+    /// Developer instructions that will be sent as a `developer` role message.
+    #[serde(skip_serializing_if = "Option::is_none")]
+    pub developer_instructions: Option<String>,
+
     /// Prompt used during conversation compaction.
     #[serde(skip_serializing_if = "Option::is_none")]
     pub compact_prompt: Option<String>,
@@ -1129,6 +1133,7 @@ mod tests {
                 sandbox: None,
                 config: None,
                 base_instructions: None,
+                developer_instructions: None,
                 compact_prompt: None,
                 include_apply_patch_tool: None,
             },
diff --git a/codex-rs/app-server/src/codex_message_processor.rs b/codex-rs/app-server/src/codex_message_processor.rs
index 14418fb048..193b47ea5a 100644
--- a/codex-rs/app-server/src/codex_message_processor.rs
+++ b/codex-rs/app-server/src/codex_message_processor.rs
@@ -1760,6 +1760,7 @@ async fn derive_config_from_params(
         sandbox: sandbox_mode,
         config: cli_overrides,
         base_instructions,
+        developer_instructions,
         compact_prompt,
         include_apply_patch_tool,
     } = params;
@@ -1773,6 +1774,7 @@ async fn derive_config_from_params(
         model_provider,
         codex_linux_sandbox_exe,
         base_instructions,
+        developer_instructions,
         compact_prompt,
         include_apply_patch_tool,
         include_view_image_tool: None,
diff --git a/codex-rs/app-server/tests/suite/send_message.rs b/codex-rs/app-server/tests/suite/send_message.rs
index 32c408dce6..8793caafcc 100644
--- a/codex-rs/app-server/tests/suite/send_message.rs
+++ b/codex-rs/app-server/tests/suite/send_message.rs
@@ -44,7 +44,9 @@ async fn test_send_message_success() -> Result<()> {
 
     // Start a conversation using the new wire API.
     let new_conv_id = mcp
-        .send_new_conversation_request(NewConversationParams::default())
+        .send_new_conversation_request(NewConversationParams {
+            ..Default::default()
+        })
         .await?;
     let new_conv_resp: JSONRPCResponse = timeout(
         DEFAULT_READ_TIMEOUT,
@@ -143,7 +145,10 @@ async fn test_send_message_raw_notifications_opt_in() -> Result<()> {
     timeout(DEFAULT_READ_TIMEOUT, mcp.initialize()).await??;
 
     let new_conv_id = mcp
-        .send_new_conversation_request(NewConversationParams::default())
+        .send_new_conversation_request(NewConversationParams {
+            developer_instructions: Some("Use the test harness tools.".to_string()),
+            ..Default::default()
+        })
         .await?;
     let new_conv_resp: JSONRPCResponse = timeout(
         DEFAULT_READ_TIMEOUT,
@@ -177,6 +182,9 @@ async fn test_send_message_raw_notifications_opt_in() -> Result<()> {
         })
         .await?;
 
+    let developer = read_raw_response_item(&mut mcp, conversation_id).await;
+    assert_developer_message(&developer, "Use the test harness tools.");
+
     let instructions = read_raw_response_item(&mut mcp, conversation_id).await;
     assert_instructions_message(&instructions);
 
@@ -316,6 +324,21 @@ fn assert_instructions_message(item: &ResponseItem) {
     }
 }
 
+fn assert_developer_message(item: &ResponseItem, expected_text: &str) {
+    match item {
+        ResponseItem::Message { role, content, .. } => {
+            assert_eq!(role, "developer");
+            let texts = content_texts(content);
+            assert_eq!(
+                texts,
+                vec![expected_text],
+                "expected developer instructions message, got {texts:?}"
+            );
+        }
+        other => panic!("expected developer instructions message, got {other:?}"),
+    }
+}
+
 fn assert_environment_message(item: &ResponseItem) {
     match item {
         ResponseItem::Message { role, content, .. } => {
diff --git a/codex-rs/core/src/codex.rs b/codex-rs/core/src/codex.rs
index e7fde7b99a..f7a5d92bf5 100644
--- a/codex-rs/core/src/codex.rs
+++ b/codex-rs/core/src/codex.rs
@@ -112,6 +112,7 @@ use crate::tools::spec::ToolsConfig;
 use crate::tools::spec::ToolsConfigParams;
 use crate::turn_diff_tracker::TurnDiffTracker;
 use crate::unified_exec::UnifiedExecSessionManager;
+use crate::user_instructions::DeveloperInstructions;
 use crate::user_instructions::UserInstructions;
 use crate::user_notification::UserNotification;
 use crate::util::backoff;
@@ -171,6 +172,7 @@ impl Codex {
             model: config.model.clone(),
             model_reasoning_effort: config.model_reasoning_effort,
             model_reasoning_summary: config.model_reasoning_summary,
+            developer_instructions: config.developer_instructions.clone(),
             user_instructions,
             base_instructions: config.base_instructions.clone(),
             compact_prompt: config.compact_prompt.clone(),
@@ -265,6 +267,7 @@ pub(crate) struct TurnContext {
     /// the model as well as sandbox policies are resolved against this path
     /// instead of `std::env::current_dir()`.
     pub(crate) cwd: PathBuf,
+    pub(crate) developer_instructions: Option<String>,
     pub(crate) base_instructions: Option<String>,
     pub(crate) compact_prompt: Option<String>,
     pub(crate) user_instructions: Option<String>,
@@ -303,6 +306,9 @@ pub(crate) struct SessionConfiguration {
     model_reasoning_effort: Option<ReasoningEffortConfig>,
     model_reasoning_summary: ReasoningSummaryConfig,
 
+    /// Developer instructions that supplement the base instructions.
+    developer_instructions: Option<String>,
+
     /// Model instructions that are appended to the base instructions.
     user_instructions: Option<String>,
 
@@ -417,6 +423,7 @@ impl Session {
             sub_id,
             client,
             cwd: session_configuration.cwd.clone(),
+            developer_instructions: session_configuration.developer_instructions.clone(),
             base_instructions: session_configuration.base_instructions.clone(),
             compact_prompt: session_configuration.compact_prompt.clone(),
             user_instructions: session_configuration.user_instructions.clone(),
@@ -991,7 +998,10 @@ impl Session {
     }
 
     pub(crate) fn build_initial_context(&self, turn_context: &TurnContext) -> Vec<ResponseItem> {
-        let mut items = Vec::<ResponseItem>::with_capacity(2);
+        let mut items = Vec::<ResponseItem>::with_capacity(3);
+        if let Some(developer_instructions) = turn_context.developer_instructions.as_deref() {
+            items.push(DeveloperInstructions::new(developer_instructions.to_string()).into());
+        }
         if let Some(user_instructions) = turn_context.user_instructions.as_deref() {
             items.push(UserInstructions::new(user_instructions.to_string()).into());
         }
@@ -1674,6 +1684,7 @@ async fn spawn_review_thread(
         sub_id: sub_id.to_string(),
         client,
         tools_config,
+        developer_instructions: None,
         user_instructions: None,
         base_instructions: Some(base_instructions.clone()),
         compact_prompt: parent_turn_context.compact_prompt.clone(),
@@ -2511,6 +2522,7 @@ mod tests {
             model: config.model.clone(),
             model_reasoning_effort: config.model_reasoning_effort,
             model_reasoning_summary: config.model_reasoning_summary,
+            developer_instructions: config.developer_instructions.clone(),
             user_instructions: config.user_instructions.clone(),
             base_instructions: config.base_instructions.clone(),
             compact_prompt: config.compact_prompt.clone(),
@@ -2586,6 +2598,7 @@ mod tests {
             model: config.model.clone(),
             model_reasoning_effort: config.model_reasoning_effort,
             model_reasoning_summary: config.model_reasoning_summary,
+            developer_instructions: config.developer_instructions.clone(),
             user_instructions: config.user_instructions.clone(),
             base_instructions: config.base_instructions.clone(),
             compact_prompt: config.compact_prompt.clone(),
diff --git a/codex-rs/core/src/config/mod.rs b/codex-rs/core/src/config/mod.rs
index b6bc9baf57..17fddcf3d3 100644
--- a/codex-rs/core/src/config/mod.rs
+++ b/codex-rs/core/src/config/mod.rs
@@ -128,6 +128,9 @@ pub struct Config {
     /// Base instructions override.
     pub base_instructions: Option<String>,
 
+    /// Developer instructions override injected as a separate message.
+    pub developer_instructions: Option<String>,
+
     /// Compact prompt override.
     pub compact_prompt: Option<String>,
 
@@ -543,6 +546,11 @@ pub struct ConfigToml {
 
     /// System instructions.
     pub instructions: Option<String>,
+
+    /// Developer instructions inserted as a `developer` role message.
+    #[serde(default)]
+    pub developer_instructions: Option<String>,
+
     /// Compact prompt used for history compaction.
     pub compact_prompt: Option<String>,
 
@@ -830,6 +838,7 @@ pub struct ConfigOverrides {
     pub config_profile: Option<String>,
     pub codex_linux_sandbox_exe: Option<PathBuf>,
     pub base_instructions: Option<String>,
+    pub developer_instructions: Option<String>,
     pub compact_prompt: Option<String>,
     pub include_apply_patch_tool: Option<bool>,
     pub include_view_image_tool: Option<bool>,
@@ -861,6 +870,7 @@ impl Config {
             config_profile: config_profile_key,
             codex_linux_sandbox_exe,
             base_instructions,
+            developer_instructions,
             compact_prompt,
             include_apply_patch_tool: include_apply_patch_tool_override,
             include_view_image_tool: include_view_image_tool_override,
@@ -1060,6 +1070,7 @@ impl Config {
             "experimental instructions file",
         )?;
         let base_instructions = base_instructions.or(file_base_instructions);
+        let developer_instructions = developer_instructions.or(cfg.developer_instructions);
 
         let experimental_compact_prompt_path = config_profile
             .experimental_compact_prompt_file
@@ -1095,6 +1106,7 @@ impl Config {
             notify: cfg.notify,
             user_instructions,
             base_instructions,
+            developer_instructions,
             compact_prompt,
             // The config.toml omits "_mode" because it's a config file. However, "_mode"
             // is important in code to differentiate the mode from the store implementation.
@@ -2886,6 +2898,7 @@ model_verbosity = "high"
                 model_verbosity: None,
                 chatgpt_base_url: "https://chatgpt.com/backend-api/".to_string(),
                 base_instructions: None,
+                developer_instructions: None,
                 compact_prompt: None,
                 forced_chatgpt_workspace_id: None,
                 forced_login_method: None,
@@ -2958,6 +2971,7 @@ model_verbosity = "high"
             model_verbosity: None,
             chatgpt_base_url: "https://chatgpt.com/backend-api/".to_string(),
             base_instructions: None,
+            developer_instructions: None,
             compact_prompt: None,
             forced_chatgpt_workspace_id: None,
             forced_login_method: None,
@@ -3045,6 +3059,7 @@ model_verbosity = "high"
             model_verbosity: None,
             chatgpt_base_url: "https://chatgpt.com/backend-api/".to_string(),
             base_instructions: None,
+            developer_instructions: None,
             compact_prompt: None,
             forced_chatgpt_workspace_id: None,
             forced_login_method: None,
@@ -3118,6 +3133,7 @@ model_verbosity = "high"
             model_verbosity: Some(Verbosity::High),
             chatgpt_base_url: "https://chatgpt.com/backend-api/".to_string(),
             base_instructions: None,
+            developer_instructions: None,
             compact_prompt: None,
             forced_chatgpt_workspace_id: None,
             forced_login_method: None,
diff --git a/codex-rs/core/src/user_instructions.rs b/codex-rs/core/src/user_instructions.rs
index 76054edcb3..f479846168 100644
--- a/codex-rs/core/src/user_instructions.rs
+++ b/codex-rs/core/src/user_instructions.rs
@@ -40,3 +40,31 @@ impl From<UserInstructions> for ResponseItem {
         }
     }
 }
+
+#[derive(Debug, Clone, Serialize, Deserialize, PartialEq)]
+#[serde(rename = "developer_instructions", rename_all = "snake_case")]
+pub(crate) struct DeveloperInstructions {
+    text: String,
+}
+
+impl DeveloperInstructions {
+    pub fn new<T: Into<String>>(text: T) -> Self {
+        Self { text: text.into() }
+    }
+
+    pub fn into_text(self) -> String {
+        self.text
+    }
+}
+
+impl From<DeveloperInstructions> for ResponseItem {
+    fn from(di: DeveloperInstructions) -> Self {
+        ResponseItem::Message {
+            id: None,
+            role: "developer".to_string(),
+            content: vec![ContentItem::InputText {
+                text: di.into_text(),
+            }],
+        }
+    }
+}
diff --git a/codex-rs/core/tests/suite/client.rs b/codex-rs/core/tests/suite/client.rs
index c1354a6257..07bee704f4 100644
--- a/codex-rs/core/tests/suite/client.rs
+++ b/codex-rs/core/tests/suite/client.rs
@@ -58,6 +58,18 @@ fn assert_message_role(request_body: &serde_json::Value, role: &str) {
     assert_eq!(request_body["role"].as_str().unwrap(), role);
 }
 
+#[expect(clippy::expect_used)]
+fn assert_message_equals(request_body: &serde_json::Value, text: &str) {
+    let content = request_body["content"][0]["text"]
+        .as_str()
+        .expect("invalid message content");
+
+    assert_eq!(
+        content, text,
+        "expected message content '{content}' to equal '{text}'"
+    );
+}
+
 #[expect(clippy::expect_used)]
 fn assert_message_starts_with(request_body: &serde_json::Value, text: &str) {
     let content = request_body["content"][0]["text"]
@@ -608,6 +620,64 @@ async fn includes_user_instructions_message_in_request() {
     assert_message_ends_with(&request_body["input"][1], "</environment_context>");
 }
 
+#[tokio::test(flavor = "multi_thread", worker_threads = 2)]
+async fn includes_developer_instructions_message_in_request() {
+    skip_if_no_network!();
+    let server = MockServer::start().await;
+
+    let resp_mock =
+        responses::mount_sse_once_match(&server, path("/v1/responses"), sse_completed("resp1"))
+            .await;
+
+    let model_provider = ModelProviderInfo {
+        base_url: Some(format!("{}/v1", server.uri())),
+        ..built_in_model_providers()["openai"].clone()
+    };
+
+    let codex_home = TempDir::new().unwrap();
+    let mut config = load_default_config_for_test(&codex_home);
+    config.model_provider = model_provider;
+    config.user_instructions = Some("be nice".to_string());
+    config.developer_instructions = Some("be useful".to_string());
+
+    let conversation_manager =
+        ConversationManager::with_auth(CodexAuth::from_api_key("Test API Key"));
+    let codex = conversation_manager
+        .new_conversation(config)
+        .await
+        .expect("create new conversation")
+        .conversation;
+
+    codex
+        .submit(Op::UserInput {
+            items: vec![UserInput::Text {
+                text: "hello".into(),
+            }],
+        })
+        .await
+        .unwrap();
+
+    wait_for_event(&codex, |ev| matches!(ev, EventMsg::TaskComplete(_))).await;
+
+    let request = resp_mock.single_request();
+    let request_body = request.body_json();
+
+    assert!(
+        !request_body["instructions"]
+            .as_str()
+            .unwrap()
+            .contains("be nice")
+    );
+    assert_message_role(&request_body["input"][0], "developer");
+    assert_message_equals(&request_body["input"][0], "be useful");
+    assert_message_role(&request_body["input"][1], "user");
+    assert_message_starts_with(&request_body["input"][1], "<user_instructions>");
+    assert_message_ends_with(&request_body["input"][1], "</user_instructions>");
+    assert_message_role(&request_body["input"][2], "user");
+    assert_message_starts_with(&request_body["input"][2], "<environment_context>");
+    assert_message_ends_with(&request_body["input"][2], "</environment_context>");
+}
+
 #[tokio::test(flavor = "multi_thread", worker_threads = 2)]
 async fn azure_responses_request_includes_store_and_reasoning_ids() {
     skip_if_no_network!();
diff --git a/codex-rs/exec/src/lib.rs b/codex-rs/exec/src/lib.rs
index 4ab0b0302b..a086990dff 100644
--- a/codex-rs/exec/src/lib.rs
+++ b/codex-rs/exec/src/lib.rs
@@ -174,6 +174,7 @@ pub async fn run_main(cli: Cli, codex_linux_sandbox_exe: Option<PathBuf>) -> any
         model_provider,
         codex_linux_sandbox_exe,
         base_instructions: None,
+        developer_instructions: None,
         compact_prompt: None,
         include_apply_patch_tool: None,
         include_view_image_tool: None,
diff --git a/codex-rs/mcp-server/src/codex_tool_config.rs b/codex-rs/mcp-server/src/codex_tool_config.rs
index 471d65603a..fd671ea12c 100644
--- a/codex-rs/mcp-server/src/codex_tool_config.rs
+++ b/codex-rs/mcp-server/src/codex_tool_config.rs
@@ -50,6 +50,10 @@ pub struct CodexToolCallParam {
     #[serde(default, skip_serializing_if = "Option::is_none")]
     pub base_instructions: Option<String>,
 
+    /// Developer instructions that should be injected as a developer role message.
+    #[serde(default, skip_serializing_if = "Option::is_none")]
+    pub developer_instructions: Option<String>,
+
     /// Prompt used when compacting the conversation.
     #[serde(default, skip_serializing_if = "Option::is_none")]
     pub compact_prompt: Option<String>,
@@ -145,6 +149,7 @@ impl CodexToolCallParam {
             sandbox,
             config: cli_overrides,
             base_instructions,
+            developer_instructions,
             compact_prompt,
         } = self;
 
@@ -159,6 +164,7 @@ impl CodexToolCallParam {
             model_provider: None,
             codex_linux_sandbox_exe,
             base_instructions,
+            developer_instructions,
             compact_prompt,
             include_apply_patch_tool: None,
             include_view_image_tool: None,
@@ -294,6 +300,10 @@ mod tests {
                 "description": "The set of instructions to use instead of the default ones.",
                 "type": "string"
               },
+              "developer-instructions": {
+                "description": "Developer instructions that should be injected as a developer role message.",
+                "type": "string"
+              },
               "compact-prompt": {
                 "description": "Prompt used when compacting the conversation.",
                 "type": "string"
diff --git a/codex-rs/mcp-server/tests/suite/codex_tool.rs b/codex-rs/mcp-server/tests/suite/codex_tool.rs
index 4ab83ca24e..ae0c23f1d8 100644
--- a/codex-rs/mcp-server/tests/suite/codex_tool.rs
+++ b/codex-rs/mcp-server/tests/suite/codex_tool.rs
@@ -341,6 +341,7 @@ async fn codex_tool_passes_base_instructions() -> anyhow::Result<()> {
         .send_codex_tool_call(CodexToolCallParam {
             prompt: "How are you?".to_string(),
             base_instructions: Some("You are a helpful assistant.".to_string()),
+            developer_instructions: Some("Foreshadow upcoming tool calls.".to_string()),
             ..Default::default()
         })
         .await?;
@@ -367,10 +368,28 @@ async fn codex_tool_passes_base_instructions() -> anyhow::Result<()> {
     );
 
     let requests = server.received_requests().await.unwrap();
-    let request = requests[0].body_json::<serde_json::Value>().unwrap();
+    let request = requests[0].body_json::<serde_json::Value>()?;
     let instructions = request["messages"][0]["content"].as_str().unwrap();
     assert!(instructions.starts_with("You are a helpful assistant."));
 
+    let developer_msg = request["messages"]
+        .as_array()
+        .and_then(|messages| {
+            messages
+                .iter()
+                .find(|msg| msg.get("role").and_then(|role| role.as_str()) == Some("developer"))
+        })
+        .unwrap();
+    let developer_content = developer_msg
+        .get("content")
+        .and_then(|value| value.as_str())
+        .unwrap();
+    assert!(
+        !developer_content.contains('<'),
+        "expected developer instructions without XML tags, got `{developer_content}`"
+    );
+    assert_eq!(developer_content, "Foreshadow upcoming tool calls.");
+
     Ok(())
 }
 
diff --git a/codex-rs/tui/src/lib.rs b/codex-rs/tui/src/lib.rs
index 0629dd8c07..487b687a57 100644
--- a/codex-rs/tui/src/lib.rs
+++ b/codex-rs/tui/src/lib.rs
@@ -144,6 +144,7 @@ pub async fn run_main(
         config_profile: cli.config_profile.clone(),
         codex_linux_sandbox_exe,
         base_instructions: None,
+        developer_instructions: None,
         compact_prompt: None,
         include_apply_patch_tool: None,
         include_view_image_tool: None,