diff --git a/codex-rs/core/src/chat_completions.rs b/codex-rs/core/src/chat_completions.rs
index 3042ec45..5ede774b 100644
--- a/codex-rs/core/src/chat_completions.rs
+++ b/codex-rs/core/src/chat_completions.rs
@@ -40,6 +40,10 @@ pub(crate) async fn stream_chat_completions(
     let full_instructions = prompt.get_full_instructions(model);
     messages.push(json!({"role": "system", "content": full_instructions}));
 
+    if let Some(instr) = &prompt.user_instructions {
+        messages.push(json!({"role": "user", "content": instr}));
+    }
+
     for item in &prompt.input {
         match item {
             ResponseItem::Message { role, content, .. } => {
diff --git a/codex-rs/core/src/client.rs b/codex-rs/core/src/client.rs
index 72104da2..4e0e62c0 100644
--- a/codex-rs/core/src/client.rs
+++ b/codex-rs/core/src/client.rs
@@ -35,6 +35,7 @@ use crate::error::Result;
 use crate::flags::CODEX_RS_SSE_FIXTURE;
 use crate::model_provider_info::ModelProviderInfo;
 use crate::model_provider_info::WireApi;
+use crate::models::ContentItem;
 use crate::models::ResponseItem;
 use crate::openai_tools::create_tools_json_for_responses_api;
 use crate::protocol::TokenUsage;
@@ -156,10 +157,20 @@ impl ModelClient {
             vec![]
         };
 
+        let mut input_with_instructions = Vec::with_capacity(prompt.input.len() + 1);
+        if let Some(ui) = &prompt.user_instructions {
+            input_with_instructions.push(ResponseItem::Message {
+                id: None,
+                role: "user".to_string(),
+                content: vec![ContentItem::InputText { text: ui.clone() }],
+            });
+        }
+        input_with_instructions.extend(prompt.input.clone());
+
         let payload = ResponsesApiRequest {
             model: &self.config.model,
             instructions: &full_instructions,
-            input: &prompt.input,
+            input: &input_with_instructions,
             tools: &tools_json,
             tool_choice: "auto",
             parallel_tool_calls: false,
diff --git a/codex-rs/core/src/client_common.rs b/codex-rs/core/src/client_common.rs
index afd2f045..157f3587 100644
--- a/codex-rs/core/src/client_common.rs
+++ b/codex-rs/core/src/client_common.rs
@@ -44,9 +44,6 @@ impl Prompt {
             .as_deref()
             .unwrap_or(BASE_INSTRUCTIONS);
         let mut sections: Vec<&str> = vec![base];
-        if let Some(ref user) = self.user_instructions {
-            sections.push(user);
-        }
         if model.starts_with("gpt-4.1") {
             sections.push(APPLY_PATCH_TOOL_INSTRUCTIONS);
         }
@@ -188,3 +185,19 @@ impl Stream for ResponseStream {
         self.rx_event.poll_recv(cx)
     }
 }
+
+#[cfg(test)]
+mod tests {
+    use super::*;
+
+    #[test]
+    fn get_full_instructions_no_user_content() {
+        let prompt = Prompt {
+            user_instructions: Some("custom instruction".to_string()),
+            ..Default::default()
+        };
+        let expected = format!("{BASE_INSTRUCTIONS}\n{APPLY_PATCH_TOOL_INSTRUCTIONS}");
+        let full = prompt.get_full_instructions("gpt-4.1");
+        assert_eq!(full, expected);
+    }
+}
diff --git a/codex-rs/core/tests/client.rs b/codex-rs/core/tests/client.rs
index fbe63fb3..67d95cb8 100644
--- a/codex-rs/core/tests/client.rs
+++ b/codex-rs/core/tests/client.rs
@@ -257,6 +257,70 @@ async fn chatgpt_auth_sends_correct_request() {
     );
 }
 
+#[tokio::test(flavor = "multi_thread", worker_threads = 2)]
+async fn includes_user_instructions_message_in_request() {
+    #![allow(clippy::unwrap_used)]
+
+    let server = MockServer::start().await;
+
+    let first = ResponseTemplate::new(200)
+        .insert_header("content-type", "text/event-stream")
+        .set_body_raw(sse_completed("resp1"), "text/event-stream");
+
+    Mock::given(method("POST"))
+        .and(path("/v1/responses"))
+        .respond_with(first)
+        .expect(1)
+        .mount(&server)
+        .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());
+
+    let ctrl_c = std::sync::Arc::new(tokio::sync::Notify::new());
+    let CodexSpawnOk { codex, .. } = Codex::spawn(
+        config,
+        Some(CodexAuth::from_api_key("Test API Key".to_string())),
+        ctrl_c.clone(),
+    )
+    .await
+    .unwrap();
+
+    codex
+        .submit(Op::UserInput {
+            items: vec![InputItem::Text {
+                text: "hello".into(),
+            }],
+        })
+        .await
+        .unwrap();
+
+    wait_for_event(&codex, |ev| matches!(ev, EventMsg::TaskComplete(_))).await;
+
+    let request = &server.received_requests().await.unwrap()[0];
+    let request_body = request.body_json::<serde_json::Value>().unwrap();
+
+    assert!(
+        !request_body["instructions"]
+            .as_str()
+            .unwrap()
+            .contains("be nice")
+    );
+    assert_eq!(request_body["input"][0]["role"], "user");
+    assert!(
+        request_body["input"][0]["content"][0]["text"]
+            .as_str()
+            .unwrap()
+            .starts_with("be nice")
+    );
+}
 fn auth_from_token(id_token: String) -> CodexAuth {
     CodexAuth::new(
         None,