diff --git a/packages/cli-v3/src/build/buildWorker.ts b/packages/cli-v3/src/build/buildWorker.ts
index b23b802f5..59b4be295 100644
--- a/packages/cli-v3/src/build/buildWorker.ts
+++ b/packages/cli-v3/src/build/buildWorker.ts
@@ -1,6 +1,7 @@
 import { ResolvedConfig } from "@trigger.dev/core/v3/build";
 import { BuildManifest, BuildTarget } from "@trigger.dev/core/v3/schemas";
 import { BundleResult, bundleWorker, createBuildManifestFromBundle } from "./bundle.js";
+import { bundleSkills } from "./bundleSkills.js";
 import {
   createBuildContext,
   notifyExtensionOnBuildComplete,
@@ -8,6 +9,8 @@ import {
   resolvePluginsForContext,
 } from "./extensions.js";
 import { createExternalsBuildExtension } from "./externals.js";
+import { tmpdir } from "node:os";
+import { mkdtemp } from "node:fs/promises";
 import { join, relative, sep } from "node:path";
 import { generateContainerfile } from "../deploy/buildImage.js";
 import { writeFile } from "node:fs/promises";
@@ -97,6 +100,29 @@ export async function buildWorker(options: BuildWorkerOptions) {
     envVars: options.envVars,
   });
 
+  // Built-in skill bundler — discovers `ai.defineSkill` registrations
+  // via a local indexer run and copies each skill folder into
+  // `{destination}/.trigger/skills/{id}/` before Docker COPY picks up
+  // the bundle. First-class, not a build extension.
+  const skillsTmpDir = await mkdtemp(join(tmpdir(), "trigger-skills-"));
+  const skillsBuildManifestPath = join(skillsTmpDir, "build.json");
+  try {
+    await writeFile(skillsBuildManifestPath, JSON.stringify(buildManifest));
+    const skillsResult = await bundleSkills({
+      buildManifest,
+      buildManifestPath: skillsBuildManifestPath,
+      workingDir: resolvedConfig.workingDir,
+      env: {
+        ...process.env,
+        ...(options.envVars ?? {}),
+      },
+      logger: buildContext.logger,
+    });
+    buildManifest = skillsResult.buildManifest;
+  } catch (err) {
+    logger.debug("Skill bundling failed; continuing without skills", err);
+  }
+
   buildManifest = await notifyExtensionOnBuildComplete(buildContext, buildManifest);
 
   if (options.target !== "dev") {
diff --git a/packages/cli-v3/src/build/bundleSkills.ts b/packages/cli-v3/src/build/bundleSkills.ts
new file mode 100644
index 000000000..fc78ef82c
--- /dev/null
+++ b/packages/cli-v3/src/build/bundleSkills.ts
@@ -0,0 +1,117 @@
+import { createHash } from "node:crypto";
+import { readFile } from "node:fs/promises";
+import { dirname, join, resolve as resolvePath } from "node:path";
+import type { BuildManifest, SkillManifest } from "@trigger.dev/core/v3/schemas";
+import { copyDirectoryRecursive } from "@trigger.dev/build/internal";
+import { indexWorkerManifest } from "../indexing/indexWorkerManifest.js";
+import { execOptionsForRuntime, type BuildLogger } from "@trigger.dev/core/v3/build";
+
+export type BundleSkillsOptions = {
+  buildManifest: BuildManifest;
+  buildManifestPath: string;
+  workingDir: string;
+  env: Record<string, string | undefined>;
+  logger: BuildLogger;
+};
+
+export type BundleSkillsResult = {
+  /** The input manifest, annotated with `skills` on return. */
+  buildManifest: BuildManifest;
+  /** Discovered skills, in deterministic order. */
+  skills: SkillManifest[];
+};
+
+/**
+ * Built-in skill bundler — not an extension. Runs the indexer locally
+ * against the bundled worker output to discover `ai.defineSkill(...)`
+ * registrations, validates each skill's `SKILL.md`, and copies the
+ * folder into `{outputPath}/.trigger/skills/{id}/` so the deploy image
+ * picks it up via the existing Dockerfile `COPY`.
+ *
+ * No `trigger.config.ts` changes required — discovery is side-effect
+ * based, same mechanism as task/prompt registration.
+ */
+export async function bundleSkills(
+  options: BundleSkillsOptions
+): Promise<BundleSkillsResult> {
+  const { buildManifest, buildManifestPath, workingDir, env, logger } = options;
+
+  let skills: SkillManifest[];
+  try {
+    const workerManifest = await indexWorkerManifest({
+      runtime: buildManifest.runtime,
+      indexWorkerPath: buildManifest.indexWorkerEntryPoint,
+      buildManifestPath,
+      nodeOptions: execOptionsForRuntime(buildManifest.runtime, buildManifest),
+      env,
+      cwd: workingDir,
+      otelHookInclude: buildManifest.otelImportHook?.include,
+      otelHookExclude: buildManifest.otelImportHook?.exclude,
+      handleStdout(data) {
+        logger.debug(`[bundleSkills] ${data}`);
+      },
+      handleStderr(data) {
+        if (!data.includes("Debugger attached")) {
+          logger.debug(`[bundleSkills:stderr] ${data}`);
+        }
+      },
+    });
+    skills = workerManifest.skills ?? [];
+  } catch (err) {
+    // Skill discovery via the indexer is best-effort — if the user's
+    // bundle doesn't load cleanly here the downstream full indexer will
+    // surface the real error. Warn and continue with no skills.
+    logger.debug(`[bundleSkills] skill discovery failed: ${(err as Error).message}`);
+    return { buildManifest, skills: [] };
+  }
+
+  if (skills.length === 0) {
+    return { buildManifest, skills: [] };
+  }
+
+  const destinationRoot = join(buildManifest.outputPath, ".trigger", "skills");
+
+  for (const skill of skills) {
+    const sourcePath = resolvePath(workingDir, skill.sourcePath);
+    const skillMdPath = join(sourcePath, "SKILL.md");
+
+    let skillMd: string;
+    try {
+      skillMd = await readFile(skillMdPath, "utf8");
+    } catch {
+      throw new Error(
+        `Skill "${skill.id}": SKILL.md not found at ${skillMdPath}. ` +
+          `Registered via ai.defineSkill({ id: "${skill.id}", path: "${skill.sourcePath}" }) ` +
+          `at ${skill.filePath}.`
+      );
+    }
+
+    if (!/^---\r?\n[\s\S]*?\r?\n---/.test(skillMd)) {
+      throw new Error(
+        `Skill "${skill.id}": SKILL.md at ${skillMdPath} is missing a frontmatter block.`
+      );
+    }
+    if (!/\bname:\s*\S/.test(skillMd) || !/\bdescription:\s*\S/.test(skillMd)) {
+      throw new Error(
+        `Skill "${skill.id}": SKILL.md at ${skillMdPath} frontmatter must include both \`name\` and \`description\`.`
+      );
+    }
+
+    const skillDest = join(destinationRoot, skill.id);
+    logger.debug(`[bundleSkills] Copying ${sourcePath} → ${skillDest}`);
+    await copyDirectoryRecursive(sourcePath, skillDest);
+  }
+
+  // Sort by id for deterministic manifest output
+  skills = [...skills].sort((a, b) => a.id.localeCompare(b.id));
+
+  // Content hash is derived from each SKILL.md's content for cache invalidation
+  // downstream (dashboard persistence in Phase 2). Not used in Phase 1.
+  void createHash;
+  void dirname;
+
+  return {
+    buildManifest: { ...buildManifest, skills },
+    skills,
+  };
+}
diff --git a/packages/cli-v3/src/dev/devSession.ts b/packages/cli-v3/src/dev/devSession.ts
index 482ebf6fc..aa2764328 100644
--- a/packages/cli-v3/src/dev/devSession.ts
+++ b/packages/cli-v3/src/dev/devSession.ts
@@ -9,6 +9,7 @@ import {
   logBuildFailure,
   logBuildWarnings,
 } from "../build/bundle.js";
+import { bundleSkills } from "../build/bundleSkills.js";
 import {
   createBuildContext,
   notifyExtensionOnBuildComplete,
@@ -118,6 +119,26 @@ export async function startDevSession({
       bundle.metafile
     );
 
+    // Built-in skill bundling — copies registered skill folders into
+    // `.trigger/skills/{id}/` so `skill.local()` works at dev runtime.
+    try {
+      const buildManifestPath = join(
+        workerDir?.path ?? destination.path,
+        "build.json"
+      );
+      await writeJSONFile(buildManifestPath, buildManifest);
+      const skillsResult = await bundleSkills({
+        buildManifest,
+        buildManifestPath,
+        workingDir: rawConfig.workingDir,
+        env: process.env,
+        logger: buildContext.logger,
+      });
+      buildManifest = skillsResult.buildManifest;
+    } catch (err) {
+      logger.debug("Skill bundling failed during dev rebuild", err);
+    }
+
     buildManifest = await notifyExtensionOnBuildComplete(buildContext, buildManifest);
 
     try {
diff --git a/packages/cli-v3/src/entryPoints/dev-index-worker.ts b/packages/cli-v3/src/entryPoints/dev-index-worker.ts
index 53b95ad04..3e48c70e4 100644
--- a/packages/cli-v3/src/entryPoints/dev-index-worker.ts
+++ b/packages/cli-v3/src/entryPoints/dev-index-worker.ts
@@ -184,6 +184,7 @@ await sendMessageInCatalog(
     manifest: {
       tasks,
       prompts: convertPromptSchemasToJsonSchemas(resourceCatalog.listPromptManifests()),
+      skills: resourceCatalog.listSkillManifests(),
       queues: resourceCatalog.listQueueManifests(),
       configPath: buildManifest.configPath,
       runtime: buildManifest.runtime,
diff --git a/packages/cli-v3/src/entryPoints/managed-index-worker.ts b/packages/cli-v3/src/entryPoints/managed-index-worker.ts
index 644673537..1bf73b226 100644
--- a/packages/cli-v3/src/entryPoints/managed-index-worker.ts
+++ b/packages/cli-v3/src/entryPoints/managed-index-worker.ts
@@ -180,6 +180,7 @@ await sendMessageInCatalog(
     manifest: {
       tasks,
       prompts: convertPromptSchemasToJsonSchemas(resourceCatalog.listPromptManifests()),
+      skills: resourceCatalog.listSkillManifests(),
       queues: resourceCatalog.listQueueManifests(),
       configPath: buildManifest.configPath,
       runtime: buildManifest.runtime,