diff --git a/codex-rs/core/src/config_loader/mod.rs b/codex-rs/core/src/config_loader/mod.rs
index d48bda18f6..d8813e23d7 100644
--- a/codex-rs/core/src/config_loader/mod.rs
+++ b/codex-rs/core/src/config_loader/mod.rs
@@ -425,7 +425,9 @@ async fn load_requirements_from_legacy_scheme(
 ///   empty array, which indicates that root detection should be disabled).
 /// - Returns an error if `project_root_markers` is specified but is not an
 ///   array of strings.
-fn project_root_markers_from_config(config: &TomlValue) -> io::Result<Option<Vec<String>>> {
+pub(crate) fn project_root_markers_from_config(
+    config: &TomlValue,
+) -> io::Result<Option<Vec<String>>> {
     let Some(table) = config.as_table() else {
         return Ok(None);
     };
@@ -454,7 +456,7 @@ fn project_root_markers_from_config(config: &TomlValue) -> io::Result<Option<Vec
     Ok(Some(markers))
 }
 
-fn default_project_root_markers() -> Vec<String> {
+pub(crate) fn default_project_root_markers() -> Vec<String> {
     DEFAULT_PROJECT_ROOT_MARKERS
         .iter()
         .map(ToString::to_string)
diff --git a/codex-rs/core/src/skills/loader.rs b/codex-rs/core/src/skills/loader.rs
index 32f1b8706e..a3c7731a6e 100644
--- a/codex-rs/core/src/skills/loader.rs
+++ b/codex-rs/core/src/skills/loader.rs
@@ -1,6 +1,9 @@
 use crate::config::Config;
 use crate::config_loader::ConfigLayerStack;
 use crate::config_loader::ConfigLayerStackOrdering;
+use crate::config_loader::default_project_root_markers;
+use crate::config_loader::merge_toml_values;
+use crate::config_loader::project_root_markers_from_config;
 use crate::skills::model::SkillDependencies;
 use crate::skills::model::SkillError;
 use crate::skills::model::SkillInterface;
@@ -20,6 +23,7 @@ use std::fs;
 use std::path::Component;
 use std::path::Path;
 use std::path::PathBuf;
+use toml::Value as TomlValue;
 use tracing::error;
 
 #[derive(Debug, Deserialize)]
@@ -72,6 +76,7 @@ struct DependencyTool {
 }
 
 const SKILLS_FILENAME: &str = "SKILL.md";
+const AGENTS_DIR_NAME: &str = ".agents";
 const SKILLS_METADATA_DIR: &str = "agents";
 const SKILLS_METADATA_FILENAME: &str = "openai.yaml";
 const SKILLS_DIR_NAME: &str = "skills";
@@ -209,15 +214,104 @@ fn skill_roots_from_layer_stack_inner(config_layer_stack: &ConfigLayerStack) ->
 }
 
 fn skill_roots(config: &Config) -> Vec<SkillRoot> {
-    skill_roots_from_layer_stack_inner(&config.config_layer_stack)
+    skill_roots_from_layer_stack_with_agents(&config.config_layer_stack, &config.cwd)
 }
 
+#[cfg(test)]
 pub(crate) fn skill_roots_from_layer_stack(
     config_layer_stack: &ConfigLayerStack,
 ) -> Vec<SkillRoot> {
     skill_roots_from_layer_stack_inner(config_layer_stack)
 }
 
+pub(crate) fn skill_roots_from_layer_stack_with_agents(
+    config_layer_stack: &ConfigLayerStack,
+    cwd: &Path,
+) -> Vec<SkillRoot> {
+    let mut roots = skill_roots_from_layer_stack_inner(config_layer_stack);
+    roots.extend(repo_agents_skill_roots(config_layer_stack, cwd));
+    dedupe_skill_roots_by_path(&mut roots);
+    roots
+}
+
+fn dedupe_skill_roots_by_path(roots: &mut Vec<SkillRoot>) {
+    let mut seen: HashSet<PathBuf> = HashSet::new();
+    roots.retain(|root| seen.insert(root.path.clone()));
+}
+
+fn repo_agents_skill_roots(config_layer_stack: &ConfigLayerStack, cwd: &Path) -> Vec<SkillRoot> {
+    let project_root_markers = project_root_markers_from_stack(config_layer_stack);
+    let project_root = find_project_root(cwd, &project_root_markers);
+    let dirs = dirs_between_project_root_and_cwd(cwd, &project_root);
+    let mut roots = Vec::new();
+    for dir in dirs {
+        let agents_skills = dir.join(AGENTS_DIR_NAME).join(SKILLS_DIR_NAME);
+        if agents_skills.is_dir() {
+            roots.push(SkillRoot {
+                path: agents_skills,
+                scope: SkillScope::Repo,
+            });
+        }
+    }
+    roots
+}
+
+fn project_root_markers_from_stack(config_layer_stack: &ConfigLayerStack) -> Vec<String> {
+    let mut merged = TomlValue::Table(toml::map::Map::new());
+    for layer in
+        config_layer_stack.get_layers(ConfigLayerStackOrdering::LowestPrecedenceFirst, false)
+    {
+        if matches!(layer.name, ConfigLayerSource::Project { .. }) {
+            continue;
+        }
+        merge_toml_values(&mut merged, &layer.config);
+    }
+
+    match project_root_markers_from_config(&merged) {
+        Ok(Some(markers)) => markers,
+        Ok(None) => default_project_root_markers(),
+        Err(err) => {
+            tracing::warn!("invalid project_root_markers: {err}");
+            default_project_root_markers()
+        }
+    }
+}
+
+fn find_project_root(cwd: &Path, project_root_markers: &[String]) -> PathBuf {
+    if project_root_markers.is_empty() {
+        return cwd.to_path_buf();
+    }
+
+    for ancestor in cwd.ancestors() {
+        for marker in project_root_markers {
+            let marker_path = ancestor.join(marker);
+            if marker_path.exists() {
+                return ancestor.to_path_buf();
+            }
+        }
+    }
+
+    cwd.to_path_buf()
+}
+
+fn dirs_between_project_root_and_cwd(cwd: &Path, project_root: &Path) -> Vec<PathBuf> {
+    let mut dirs = cwd
+        .ancestors()
+        .scan(false, |done, a| {
+            if *done {
+                None
+            } else {
+                if a == project_root {
+                    *done = true;
+                }
+                Some(a.to_path_buf())
+            }
+        })
+        .collect::<Vec<_>>();
+    dirs.reverse();
+    dirs
+}
+
 fn discover_skills_under_root(root: &Path, scope: SkillScope, outcome: &mut SkillLoadOutcome) {
     let Ok(root) = canonicalize_path(root) else {
         return;
@@ -1615,6 +1709,40 @@ interface:
         );
     }
 
+    #[tokio::test]
+    async fn loads_skills_from_agents_dir_without_codex_dir() {
+        let codex_home = tempfile::tempdir().expect("tempdir");
+        let repo_dir = tempfile::tempdir().expect("tempdir");
+        mark_as_git_repo(repo_dir.path());
+
+        let skill_path = write_skill_at(
+            &repo_dir.path().join(AGENTS_DIR_NAME).join(SKILLS_DIR_NAME),
+            "agents",
+            "agents-skill",
+            "from agents",
+        );
+        let cfg = make_config_for_cwd(&codex_home, repo_dir.path().to_path_buf()).await;
+
+        let outcome = load_skills(&cfg);
+        assert!(
+            outcome.errors.is_empty(),
+            "unexpected errors: {:?}",
+            outcome.errors
+        );
+        assert_eq!(
+            outcome.skills,
+            vec![SkillMetadata {
+                name: "agents-skill".to_string(),
+                description: "from agents".to_string(),
+                short_description: None,
+                interface: None,
+                dependencies: None,
+                path: normalized(&skill_path),
+                scope: SkillScope::Repo,
+            }]
+        );
+    }
+
     #[tokio::test]
     async fn loads_skills_from_all_codex_dirs_under_project_root() {
         let codex_home = tempfile::tempdir().expect("tempdir");
diff --git a/codex-rs/core/src/skills/manager.rs b/codex-rs/core/src/skills/manager.rs
index 3b100991f7..85e0bf20eb 100644
--- a/codex-rs/core/src/skills/manager.rs
+++ b/codex-rs/core/src/skills/manager.rs
@@ -15,7 +15,7 @@ use crate::config_loader::LoaderOverrides;
 use crate::config_loader::load_config_layers_state;
 use crate::skills::SkillLoadOutcome;
 use crate::skills::loader::load_skills_from_roots;
-use crate::skills::loader::skill_roots_from_layer_stack;
+use crate::skills::loader::skill_roots_from_layer_stack_with_agents;
 use crate::skills::system::install_system_skills;
 
 pub struct SkillsManager {
@@ -47,7 +47,8 @@ impl SkillsManager {
             return outcome;
         }
 
-        let roots = skill_roots_from_layer_stack(&config.config_layer_stack);
+        let roots =
+            skill_roots_from_layer_stack_with_agents(&config.config_layer_stack, &config.cwd);
         let mut outcome = load_skills_from_roots(roots);
         outcome.disabled_paths = disabled_paths_from_stack(&config.config_layer_stack);
         match self.cache_by_cwd.write() {
@@ -105,7 +106,7 @@ impl SkillsManager {
             }
         };
 
-        let roots = skill_roots_from_layer_stack(&config_layer_stack);
+        let roots = skill_roots_from_layer_stack_with_agents(&config_layer_stack, cwd);
         let mut outcome = load_skills_from_roots(roots);
         outcome.disabled_paths = disabled_paths_from_stack(&config_layer_stack);
         match self.cache_by_cwd.write() {