diff --git a/src/features/rules/copilot-rule.test.ts b/src/features/rules/copilot-rule.test.ts
index bf874da96..909ae1450 100644
--- a/src/features/rules/copilot-rule.test.ts
+++ b/src/features/rules/copilot-rule.test.ts
@@ -594,6 +594,55 @@ This is test rule content from file.`;
       expect(copilotRule.isRoot()).toBe(true);
     });
 
+    it("should use relativeDirPath to distinguish non-root files named copilot-instructions.md", async () => {
+      const instructionsDir = join(testDir, ".github", "instructions");
+      await ensureDir(instructionsDir);
+
+      const fileContent = `---
+description: "Same filename as root"
+applyTo: "**/*.ts"
+---
+
+This should be treated as a non-root rule.`;
+      await writeFileContent(join(instructionsDir, "copilot-instructions.md"), fileContent);
+
+      const copilotRule = await CopilotRule.fromFile({
+        baseDir: testDir,
+        relativeDirPath: ".github/instructions",
+        relativeFilePath: "copilot-instructions.md",
+        validate: true,
+      });
+
+      expect(copilotRule.isRoot()).toBe(false);
+      expect(copilotRule.getRelativeDirPath()).toBe(".github/instructions");
+      expect(copilotRule.getRelativeFilePath()).toBe("copilot-instructions.instructions.md");
+      expect(copilotRule.getFrontmatter()).toEqual({
+        description: "Same filename as root",
+        applyTo: "**/*.ts",
+      });
+      expect(copilotRule.getBody()).toBe("This should be treated as a non-root rule.");
+    });
+
+    it("should detect root only when both relativeDirPath and filename match", async () => {
+      const githubDir = join(testDir, ".github");
+      await ensureDir(githubDir);
+
+      const rootContent = "Root detected with explicit directory.";
+      await writeFileContent(join(githubDir, "copilot-instructions.md"), rootContent);
+
+      const copilotRule = await CopilotRule.fromFile({
+        baseDir: testDir,
+        relativeDirPath: ".github",
+        relativeFilePath: "copilot-instructions.md",
+        validate: true,
+      });
+
+      expect(copilotRule.isRoot()).toBe(true);
+      expect(copilotRule.getRelativeDirPath()).toBe(".github");
+      expect(copilotRule.getRelativeFilePath()).toBe("copilot-instructions.md");
+      expect(copilotRule.getBody()).toBe(rootContent);
+    });
+
     it("should load root file from .copilot/copilot-instructions.md when global=true", async () => {
       const copilotDir = join(testDir, ".copilot");
       await ensureDir(copilotDir);
diff --git a/src/features/rules/copilot-rule.ts b/src/features/rules/copilot-rule.ts
index ee3fe625a..7599dedab 100644
--- a/src/features/rules/copilot-rule.ts
+++ b/src/features/rules/copilot-rule.ts
@@ -202,13 +202,21 @@ export class CopilotRule extends ToolRule {
 
   static async fromFile({
     baseDir = process.cwd(),
+    relativeDirPath,
     relativeFilePath,
     validate = true,
     global = false,
   }: ToolRuleFromFileParams): Promise<CopilotRule> {
     const paths = this.getSettablePaths({ global });
-    // Determine if this is a root file based on the file path
-    const isRoot = relativeFilePath === paths.root.relativeFilePath;
+    const isRoot = relativeDirPath
+      ? join(relativeDirPath, relativeFilePath) ===
+        join(paths.root.relativeDirPath, paths.root.relativeFilePath)
+      : relativeFilePath === paths.root.relativeFilePath;
+    const resolvedRelativeDirPath =
+      relativeDirPath ??
+      (isRoot
+        ? paths.root.relativeDirPath
+        : (paths.nonRoot?.relativeDirPath ?? paths.root.relativeDirPath));
 
     if (isRoot) {
       const relativePath = join(paths.root.relativeDirPath, paths.root.relativeFilePath);
@@ -230,7 +238,7 @@ export class CopilotRule extends ToolRule {
       throw new Error(`nonRoot path is not set for ${relativeFilePath}`);
     }
 
-    const relativePath = join(paths.nonRoot.relativeDirPath, relativeFilePath);
+    const relativePath = join(resolvedRelativeDirPath, relativeFilePath);
     const filePath = join(baseDir, relativePath);
     const fileContent = await readFileContent(filePath);
 
@@ -244,7 +252,7 @@ export class CopilotRule extends ToolRule {
 
     return new CopilotRule({
       baseDir: baseDir,
-      relativeDirPath: paths.nonRoot.relativeDirPath,
+      relativeDirPath: resolvedRelativeDirPath,
       relativeFilePath: relativeFilePath.endsWith(".instructions.md")
         ? relativeFilePath
         : relativeFilePath.replace(/\.md$/, ".instructions.md"),
@@ -262,7 +270,9 @@ export class CopilotRule extends ToolRule {
     global = false,
   }: ToolRuleForDeletionParams): CopilotRule {
     const paths = this.getSettablePaths({ global });
-    const isRoot = relativeFilePath === paths.root.relativeFilePath;
+    const isRoot =
+      join(relativeDirPath, relativeFilePath) ===
+      join(paths.root.relativeDirPath, paths.root.relativeFilePath);
 
     return new CopilotRule({
       baseDir,