diff --git a/rust/crates/api/src/error.rs b/rust/crates/api/src/error.rs
index 836f46e0ce..21d980af20 100644
--- a/rust/crates/api/src/error.rs
+++ b/rust/crates/api/src/error.rs
@@ -14,6 +14,11 @@ const CONTEXT_WINDOW_ERROR_MARKERS: &[&str] = &[
     "too many tokens",
     "prompt is too long",
     "input is too long",
+    "input tokens exceed",
+    "configured limit",
+    "messages resulted in",
+    "completion tokens",
+    "prompt tokens",
     "request is too large",
 ];
 
@@ -542,6 +547,26 @@ mod tests {
         assert_eq!(error.request_id(), Some("req_ctx_123"));
     }
 
+    #[test]
+    fn classifies_openai_configured_limit_errors_as_context_window_failures() {
+        let error = ApiError::Api {
+            status: reqwest::StatusCode::BAD_REQUEST,
+            error_type: Some("invalid_request_error".to_string()),
+            message: Some(
+                "Input tokens exceed the configured limit of 922000 tokens. Your messages resulted in 1860900 tokens. Please reduce the length of the messages."
+                    .to_string(),
+            ),
+            request_id: Some("req_ctx_openai_123".to_string()),
+            body: String::new(),
+            retryable: false,
+            suggested_action: None,
+        };
+
+        assert!(error.is_context_window_failure());
+        assert_eq!(error.safe_failure_class(), "context_window");
+        assert_eq!(error.request_id(), Some("req_ctx_openai_123"));
+    }
+
     #[test]
     fn missing_credentials_without_hint_renders_the_canonical_message() {
         // given
diff --git a/rust/crates/api/src/providers/mod.rs b/rust/crates/api/src/providers/mod.rs
index 86871a82a1..0ef663f183 100644
--- a/rust/crates/api/src/providers/mod.rs
+++ b/rust/crates/api/src/providers/mod.rs
@@ -252,17 +252,16 @@ pub fn detect_provider_kind(model: &str) -> ProviderKind {
 
 #[must_use]
 pub fn max_tokens_for_model(model: &str) -> u32 {
-    model_token_limit(model).map_or_else(
-        || {
-            let canonical = resolve_model_alias(model);
-            if canonical.contains("opus") {
-                32_000
-            } else {
-                64_000
-            }
-        },
-        |limit| limit.max_output_tokens,
-    )
+    let canonical = resolve_model_alias(model);
+    let heuristic = if canonical.contains("opus") {
+        32_000
+    } else {
+        64_000
+    };
+
+    model_token_limit(model)
+        .map(|limit| heuristic.min(limit.max_output_tokens))
+        .unwrap_or(heuristic)
 }
 
 /// Returns the effective max output tokens for a model, preferring a plugin
@@ -276,7 +275,8 @@ pub fn max_tokens_for_model_with_override(model: &str, plugin_override: Option<u
 #[must_use]
 pub fn model_token_limit(model: &str) -> Option<ModelTokenLimit> {
     let canonical = resolve_model_alias(model);
-    match canonical.as_str() {
+    let base_model = canonical.rsplit('/').next().unwrap_or(canonical.as_str());
+    match base_model {
         "claude-opus-4-6" => Some(ModelTokenLimit {
             max_output_tokens: 32_000,
             context_window_tokens: 200_000,
@@ -289,6 +289,20 @@ pub fn model_token_limit(model: &str) -> Option<ModelTokenLimit> {
             max_output_tokens: 64_000,
             context_window_tokens: 131_072,
         }),
+        // GPT-4.1 family via the OpenAI API.
+        "gpt-4.1" | "gpt-4.1-mini" | "gpt-4.1-nano" => Some(ModelTokenLimit {
+            max_output_tokens: 32_768,
+            context_window_tokens: 1_047_576,
+        }),
+        // GPT-5.4 family via the OpenAI API.
+        "gpt-5.4" => Some(ModelTokenLimit {
+            max_output_tokens: 128_000,
+            context_window_tokens: 1_000_000,
+        }),
+        "gpt-5.4-mini" | "gpt-5.4-nano" => Some(ModelTokenLimit {
+            max_output_tokens: 128_000,
+            context_window_tokens: 400_000,
+        }),
         // Kimi models via DashScope (Moonshot AI)
         // Source: https://platform.moonshot.cn/docs/intro
         "kimi-k2.5" | "kimi-k1.5" => Some(ModelTokenLimit {
@@ -614,6 +628,15 @@ mod tests {
     fn keeps_existing_max_token_heuristic() {
         assert_eq!(max_tokens_for_model("opus"), 32_000);
         assert_eq!(max_tokens_for_model("grok-3"), 64_000);
+        assert_eq!(max_tokens_for_model("gpt-5.4"), 64_000);
+    }
+
+    #[test]
+    fn caps_default_max_tokens_to_openai_model_limits() {
+        assert_eq!(max_tokens_for_model("gpt-4.1-mini"), 32_768);
+        assert_eq!(max_tokens_for_model("openai/gpt-4.1-mini"), 32_768);
+        assert_eq!(max_tokens_for_model("gpt-5.4"), 64_000);
+        assert_eq!(max_tokens_for_model("openai/gpt-5.4"), 64_000);
     }
 
     #[test]
@@ -680,6 +703,18 @@ mod tests {
                 .context_window_tokens,
             131_072
         );
+        assert_eq!(
+            model_token_limit("openai/gpt-4.1-mini")
+                .expect("openai/gpt-4.1-mini should be registered")
+                .context_window_tokens,
+            1_047_576
+        );
+        assert_eq!(
+            model_token_limit("gpt-5.4")
+                .expect("gpt-5.4 should be registered")
+                .context_window_tokens,
+            1_000_000
+        );
     }
 
     #[test]
@@ -728,6 +763,42 @@ mod tests {
         }
     }
 
+    #[test]
+    fn preflight_blocks_oversized_requests_for_gpt_5_4() {
+        let request = MessageRequest {
+            model: "gpt-5.4".to_string(),
+            max_tokens: 64_000,
+            messages: vec![InputMessage {
+                role: "user".to_string(),
+                content: vec![InputContentBlock::Text {
+                    text: "x".repeat(3_900_000),
+                }],
+            }],
+            system: Some("Keep the answer short.".to_string()),
+            tools: None,
+            tool_choice: None,
+            stream: true,
+            ..Default::default()
+        };
+
+        let error = preflight_message_request(&request)
+            .expect_err("oversized gpt-5.4 request should be rejected before the provider call");
+
+        match error {
+            ApiError::ContextWindowExceeded {
+                model,
+                requested_output_tokens,
+                context_window_tokens,
+                ..
+            } => {
+                assert_eq!(model, "gpt-5.4");
+                assert_eq!(requested_output_tokens, 64_000);
+                assert_eq!(context_window_tokens, 1_000_000);
+            }
+            other => panic!("expected context-window preflight failure, got {other:?}"),
+        }
+    }
+
     #[test]
     fn preflight_skips_unknown_models() {
         let request = MessageRequest {
diff --git a/rust/crates/rusty-claude-cli/src/main.rs b/rust/crates/rusty-claude-cli/src/main.rs
index dbdbd07b64..e46ec75376 100644
--- a/rust/crates/rusty-claude-cli/src/main.rs
+++ b/rust/crates/rusty-claude-cli/src/main.rs
@@ -148,11 +148,7 @@ impl ModelProvenance {
 }
 
 fn max_tokens_for_model(model: &str) -> u32 {
-    if model.contains("opus") {
-        32_000
-    } else {
-        64_000
-    }
+    api::max_tokens_for_model(model)
 }
 // Build-time constants injected by build.rs (fall back to static values when
 // build.rs hasn't run, e.g. in doc-test or unusual toolchain environments).
@@ -9424,6 +9420,39 @@ mod tests {
         );
     }
 
+    #[test]
+    fn openai_configured_limit_errors_are_rendered_as_context_window_guidance() {
+        let error = ApiError::Api {
+            status: "400".parse().expect("status"),
+            error_type: Some("invalid_request_error".to_string()),
+            message: Some(
+                "Input tokens exceed the configured limit of 922000 tokens. Your messages resulted in 1860900 tokens. Please reduce the length of the messages."
+                    .to_string(),
+            ),
+            request_id: Some("req_ctx_openai_456".to_string()),
+            body: String::new(),
+            retryable: false,
+            suggested_action: None,
+        };
+
+        let rendered = format_user_visible_api_error("session-issue-32", &error);
+        assert!(rendered.contains("Context window blocked"), "{rendered}");
+        assert!(rendered.contains("context_window_blocked"), "{rendered}");
+        assert!(
+            rendered.contains("Trace            req_ctx_openai_456"),
+            "{rendered}"
+        );
+        assert!(
+            rendered.contains("Detail           Input tokens exceed the configured limit of 922000 tokens."),
+            "{rendered}"
+        );
+        assert!(rendered.contains("Compact          /compact"), "{rendered}");
+        assert!(
+            rendered.contains("Fresh session    /clear --confirm"),
+            "{rendered}"
+        );
+    }
+
     #[test]
     fn retry_wrapped_context_window_errors_keep_recovery_guidance() {
         let error = ApiError::RetriesExhausted {