diff --git a/packages/nitro/package.json b/packages/nitro/package.json
index 2f5ee0d52fa8..54dab47a7157 100644
--- a/packages/nitro/package.json
+++ b/packages/nitro/package.json
@@ -38,13 +38,14 @@
     "nitro": ">=3.0.0-0 <4.0.0 || 3.0.260311-beta || 3.0.260415-beta"
   },
   "dependencies": {
+    "@sentry/bundler-plugin-core": "^5.2.0",
     "@sentry/core": "10.49.0",
     "@sentry/node": "10.49.0",
     "@sentry/opentelemetry": "10.49.0"
   },
   "devDependencies": {
-    "h3": "^2.0.1-rc.13",
-    "nitro": "^3.0.260415-beta"
+    "nitro": "^3.0.260415-beta",
+    "h3": "^2.0.1-rc.13"
   },
   "scripts": {
     "build": "run-p build:transpile build:types",
diff --git a/packages/nitro/rollup.npm.config.mjs b/packages/nitro/rollup.npm.config.mjs
index 1e41829a3a3a..3be46cb5f15b 100644
--- a/packages/nitro/rollup.npm.config.mjs
+++ b/packages/nitro/rollup.npm.config.mjs
@@ -5,7 +5,7 @@ export default [
     makeBaseNPMConfig({
       entrypoints: ['src/index.ts', 'src/runtime/plugins/server.ts'],
       packageSpecificConfig: {
-        external: [/^nitro/, /^h3/, /^srvx/, /^@sentry\/opentelemetry/],
+        external: [/^nitro/, /^h3/, /^srvx/, /^@sentry\/opentelemetry/, '@sentry/bundler-plugin-core'],
       },
     }),
   ),
diff --git a/packages/nitro/src/config.ts b/packages/nitro/src/config.ts
index 219eb453fb18..cdc0f2b00dfb 100644
--- a/packages/nitro/src/config.ts
+++ b/packages/nitro/src/config.ts
@@ -1,18 +1,15 @@
+import type { BuildTimeOptionsBase } from '@sentry/core';
 import type { NitroConfig } from 'nitro/types';
 import { createNitroModule } from './module';
+import { configureSourcemapSettings } from './sourceMaps';
 
-type SentryNitroOptions = {
-  // TODO: Add options
-};
+export type SentryNitroOptions = BuildTimeOptionsBase;
 
 /**
  * Modifies the passed in Nitro configuration with automatic build-time instrumentation.
- *
- * @param config A Nitro configuration object, as usually exported in `nitro.config.ts` or `nitro.config.mjs`.
- * @returns The modified config to be exported
  */
-export function withSentryConfig(config: NitroConfig, moduleOptions?: SentryNitroOptions): NitroConfig {
-  return setupSentryNitroModule(config, moduleOptions);
+export function withSentryConfig(config: NitroConfig, sentryOptions?: SentryNitroOptions): NitroConfig {
+  return setupSentryNitroModule(config, sentryOptions);
 }
 
 /**
@@ -20,15 +17,17 @@ export function withSentryConfig(config: NitroConfig, moduleOptions?: SentryNitr
  */
 export function setupSentryNitroModule(
   config: NitroConfig,
-  _moduleOptions?: SentryNitroOptions,
+  moduleOptions?: SentryNitroOptions,
   _serverConfigFile?: string,
 ): NitroConfig {
   if (!config.tracingChannel) {
     config.tracingChannel = true;
   }
 
+  const { sentryEnabledSourcemaps } = configureSourcemapSettings(config, moduleOptions);
+
   config.modules = config.modules || [];
-  config.modules.push(createNitroModule());
+  config.modules.push(createNitroModule(moduleOptions, sentryEnabledSourcemaps));
 
   return config;
 }
diff --git a/packages/nitro/src/module.ts b/packages/nitro/src/module.ts
index 1f0955301813..1a4e5b0478d1 100644
--- a/packages/nitro/src/module.ts
+++ b/packages/nitro/src/module.ts
@@ -1,14 +1,17 @@
 import type { NitroModule } from 'nitro/types';
+import type { SentryNitroOptions } from './config';
 import { instrumentServer } from './instruments/instrumentServer';
+import { setupSourceMaps } from './sourceMaps';
 
 /**
  * Creates a Nitro module to setup the Sentry SDK.
  */
-export function createNitroModule(): NitroModule {
+export function createNitroModule(sentryOptions?: SentryNitroOptions, sentryEnabledSourcemaps?: boolean): NitroModule {
   return {
     name: 'sentry',
     setup: nitro => {
       instrumentServer(nitro);
+      setupSourceMaps(nitro, sentryOptions, sentryEnabledSourcemaps);
     },
   };
 }
diff --git a/packages/nitro/src/sourceMaps.ts b/packages/nitro/src/sourceMaps.ts
new file mode 100644
index 000000000000..baaad94b658f
--- /dev/null
+++ b/packages/nitro/src/sourceMaps.ts
@@ -0,0 +1,158 @@
+import type { Options as BundlerPluginOptions } from '@sentry/bundler-plugin-core';
+import { createSentryBuildPluginManager } from '@sentry/bundler-plugin-core';
+import type { Nitro, NitroConfig } from 'nitro/types';
+import type { SentryNitroOptions } from './config';
+
+/**
+ * Registers a `compiled` hook to upload source maps after the build completes.
+ */
+export function setupSourceMaps(nitro: Nitro, options?: SentryNitroOptions, sentryEnabledSourcemaps?: boolean): void {
+  // The `compiled` hook fires on EVERY rebuild during `nitro dev` watch mode.
+  // nitro.options.dev is reliably set by the time module setup runs.
+  if (nitro.options.dev) {
+    return;
+  }
+
+  // Nitro spawns a nested Nitro instance for prerendering with the user's `modules` re-installed.
+  // Uploading here would double-upload source maps and create a duplicate release.
+  if (nitro.options.preset === 'nitro-prerender') {
+    return;
+  }
+
+  // Respect user's explicit disable
+  if (options?.sourcemaps?.disable === true) {
+    return;
+  }
+
+  nitro.hooks.hook('compiled', async (_nitro: Nitro) => {
+    await handleSourceMapUpload(_nitro, options, sentryEnabledSourcemaps);
+  });
+}
+
+/**
+ * Handles the actual source map upload after the build completes.
+ */
+async function handleSourceMapUpload(
+  nitro: Nitro,
+  options?: SentryNitroOptions,
+  sentryEnabledSourcemaps?: boolean,
+): Promise<void> {
+  const outputDir = nitro.options.output.serverDir;
+  const pluginOptions = getPluginOptions(options, sentryEnabledSourcemaps);
+
+  const sentryBuildPluginManager = createSentryBuildPluginManager(pluginOptions, {
+    buildTool: 'nitro',
+    loggerPrefix: '[@sentry/nitro]',
+  });
+
+  await sentryBuildPluginManager.telemetry.emitBundlerPluginExecutionSignal();
+  await sentryBuildPluginManager.createRelease();
+
+  await sentryBuildPluginManager.injectDebugIds([outputDir]);
+
+  if (options?.sourcemaps?.disable !== 'disable-upload') {
+    await sentryBuildPluginManager.uploadSourcemaps([outputDir], {
+      // We don't prepare the artifacts because we injected debug IDs manually before
+      prepareArtifacts: false,
+    });
+    await sentryBuildPluginManager.deleteArtifacts();
+  }
+}
+
+/**
+ * Normalizes the beginning of a path from e.g. ../../../ to ./
+ */
+function normalizePath(path: string): string {
+  return path.replace(/^(\.\.\/)+/, './');
+}
+
+/**
+ * Builds the plugin options for `createSentryBuildPluginManager` from the Sentry Nitro options.
+ *
+ * Only exported for testing purposes.
+ */
+export function getPluginOptions(
+  options?: SentryNitroOptions,
+  sentryEnabledSourcemaps?: boolean,
+): BundlerPluginOptions {
+  return {
+    org: options?.org ?? process.env.SENTRY_ORG,
+    project: options?.project ?? process.env.SENTRY_PROJECT,
+    authToken: options?.authToken ?? process.env.SENTRY_AUTH_TOKEN,
+    url: options?.sentryUrl ?? process.env.SENTRY_URL,
+    headers: options?.headers,
+    telemetry: options?.telemetry ?? true,
+    debug: options?.debug ?? false,
+    silent: options?.silent ?? false,
+    errorHandler: options?.errorHandler,
+    sourcemaps: {
+      disable: options?.sourcemaps?.disable,
+      assets: options?.sourcemaps?.assets,
+      ignore: options?.sourcemaps?.ignore,
+      filesToDeleteAfterUpload:
+        options?.sourcemaps?.filesToDeleteAfterUpload ?? (sentryEnabledSourcemaps ? ['**/*.map'] : undefined),
+      rewriteSources: options?.sourcemaps?.rewriteSources ?? ((source: string) => normalizePath(source)),
+    },
+    release: options?.release,
+    bundleSizeOptimizations: options?.bundleSizeOptimizations,
+    _metaOptions: {
+      telemetry: {
+        metaFramework: 'nitro',
+      },
+    },
+  };
+}
+
+/*  Source map configuration rules:
+    1. User explicitly disabled source maps (sourcemap: false)
+      - Keep their setting, emit a warning that errors won't be unminified in Sentry
+      - We will not upload anything
+    2. User enabled source map generation (true)
+      - Keep their setting (don't modify besides uploading)
+    3. User did not set source maps (undefined)
+      - We enable source maps for Sentry
+      - Configure `filesToDeleteAfterUpload` to clean up .map files after upload
+*/
+export function configureSourcemapSettings(
+  config: NitroConfig,
+  moduleOptions?: SentryNitroOptions,
+): { sentryEnabledSourcemaps: boolean } {
+  const sourcemapUploadDisabled = moduleOptions?.sourcemaps?.disable === true;
+  if (sourcemapUploadDisabled) {
+    return { sentryEnabledSourcemaps: false };
+  }
+
+  if (config.sourcemap === false) {
+    // eslint-disable-next-line no-console
+    console.warn(
+      '[@sentry/nitro] You have explicitly disabled source maps (`sourcemap: false`). Sentry will not upload source maps, and errors will not be unminified. To let Sentry handle source maps, remove the `sourcemap` option from your Nitro config, or use `sourcemaps: { disable: true }` in your Sentry options to silence this warning.',
+    );
+    return { sentryEnabledSourcemaps: false };
+  }
+
+  let sentryEnabledSourcemaps = false;
+  if (config.sourcemap === true) {
+    if (moduleOptions?.debug) {
+      // eslint-disable-next-line no-console
+      console.log('[@sentry/nitro] Source maps are already enabled. Sentry will upload them for error unminification.');
+    }
+  } else {
+    // User did not explicitly set sourcemap — enable it for Sentry
+    config.sourcemap = true;
+    sentryEnabledSourcemaps = true;
+    if (moduleOptions?.debug) {
+      // eslint-disable-next-line no-console
+      console.log(
+        '[@sentry/nitro] Enabled source map generation for Sentry. Source map files will be deleted after upload.',
+      );
+    }
+  }
+
+  // Nitro v3 has a `sourcemapMinify` plugin that destructively deletes `sourcesContent`,
+  // `x_google_ignoreList`, and clears `mappings` for any chunk containing `node_modules`.
+  // This makes sourcemaps unusable for Sentry.
+  config.experimental = config.experimental || {};
+  config.experimental.sourcemapMinify = false;
+
+  return { sentryEnabledSourcemaps };
+}
diff --git a/packages/nitro/test/sourceMaps.test.ts b/packages/nitro/test/sourceMaps.test.ts
new file mode 100644
index 000000000000..ffc0c0295979
--- /dev/null
+++ b/packages/nitro/test/sourceMaps.test.ts
@@ -0,0 +1,312 @@
+import type { NitroConfig } from 'nitro/types';
+import { afterEach, beforeEach, describe, expect, it, vi } from 'vitest';
+import type { SentryNitroOptions } from '../src/config';
+import { setupSentryNitroModule } from '../src/config';
+import { configureSourcemapSettings, getPluginOptions, setupSourceMaps } from '../src/sourceMaps';
+
+vi.mock('../src/instruments/instrumentServer', () => ({
+  instrumentServer: vi.fn(),
+}));
+
+describe('getPluginOptions', () => {
+  const originalEnv = process.env;
+
+  beforeEach(() => {
+    process.env = { ...originalEnv };
+  });
+
+  afterEach(() => {
+    process.env = originalEnv;
+  });
+
+  it('returns default options when no options are provided', () => {
+    const options = getPluginOptions(undefined, true);
+
+    expect(options).toEqual(
+      expect.objectContaining({
+        telemetry: true,
+        debug: false,
+        silent: false,
+        sourcemaps: expect.objectContaining({
+          filesToDeleteAfterUpload: ['**/*.map'],
+          rewriteSources: expect.any(Function),
+        }),
+        _metaOptions: expect.objectContaining({
+          telemetry: expect.objectContaining({
+            metaFramework: 'nitro',
+          }),
+        }),
+      }),
+    );
+    expect(options.org).toBeUndefined();
+    expect(options.project).toBeUndefined();
+    expect(options.authToken).toBeUndefined();
+    expect(options.url).toBeUndefined();
+  });
+
+  it('does not default filesToDeleteAfterUpload when user enabled sourcemaps themselves', () => {
+    const options = getPluginOptions(undefined, false);
+
+    expect(options.sourcemaps?.filesToDeleteAfterUpload).toBeUndefined();
+  });
+
+  it('respects user-provided filesToDeleteAfterUpload even when Sentry enabled sourcemaps', () => {
+    const options = getPluginOptions({ sourcemaps: { filesToDeleteAfterUpload: ['dist/**/*.map'] } }, true);
+
+    expect(options.sourcemaps?.filesToDeleteAfterUpload).toEqual(['dist/**/*.map']);
+  });
+
+  it('uses environment variables as fallback', () => {
+    process.env.SENTRY_ORG = 'env-org';
+    process.env.SENTRY_PROJECT = 'env-project';
+    process.env.SENTRY_AUTH_TOKEN = 'env-token';
+    process.env.SENTRY_URL = 'https://custom.sentry.io';
+
+    const options = getPluginOptions();
+
+    expect(options.org).toBe('env-org');
+    expect(options.project).toBe('env-project');
+    expect(options.authToken).toBe('env-token');
+    expect(options.url).toBe('https://custom.sentry.io'); // sentryUrl maps to url
+  });
+
+  it('prefers direct options over environment variables', () => {
+    process.env.SENTRY_ORG = 'env-org';
+    process.env.SENTRY_AUTH_TOKEN = 'env-token';
+    process.env.SENTRY_URL = 'https://env.sentry.io';
+
+    const options = getPluginOptions({
+      org: 'direct-org',
+      authToken: 'direct-token',
+      sentryUrl: 'https://direct.sentry.io',
+    });
+
+    expect(options.org).toBe('direct-org');
+    expect(options.authToken).toBe('direct-token');
+    expect(options.url).toBe('https://direct.sentry.io');
+  });
+
+  it('passes through all user options', () => {
+    const sentryOptions: SentryNitroOptions = {
+      org: 'my-org',
+      project: 'my-project',
+      authToken: 'my-token',
+      sentryUrl: 'https://my-sentry.io',
+      headers: { 'X-Custom': 'header' },
+      debug: true,
+      silent: true,
+      telemetry: false,
+      errorHandler: () => {},
+      release: { name: 'v1.0.0' },
+      sourcemaps: {
+        assets: ['dist/**'],
+        ignore: ['dist/test/**'],
+        filesToDeleteAfterUpload: ['dist/**/*.map'],
+      },
+    };
+
+    const options = getPluginOptions(sentryOptions);
+
+    expect(options.org).toBe('my-org');
+    expect(options.project).toBe('my-project');
+    expect(options.authToken).toBe('my-token');
+    expect(options.url).toBe('https://my-sentry.io');
+    expect(options.headers).toEqual({ 'X-Custom': 'header' });
+    expect(options.debug).toBe(true);
+    expect(options.silent).toBe(true);
+    expect(options.telemetry).toBe(false);
+    expect(options.errorHandler).toBeDefined();
+    expect(options.release).toEqual({ name: 'v1.0.0' });
+    expect(options.sourcemaps?.assets).toEqual(['dist/**']);
+    expect(options.sourcemaps?.ignore).toEqual(['dist/test/**']);
+    expect(options.sourcemaps?.filesToDeleteAfterUpload).toEqual(['dist/**/*.map']);
+  });
+
+  it('normalizes source paths via rewriteSources', () => {
+    const options = getPluginOptions();
+    const rewriteSources = options.sourcemaps?.rewriteSources;
+
+    expect(rewriteSources?.('../../../src/index.ts', undefined)).toBe('./src/index.ts');
+    expect(rewriteSources?.('../../lib/utils.ts', undefined)).toBe('./lib/utils.ts');
+    expect(rewriteSources?.('./src/index.ts', undefined)).toBe('./src/index.ts');
+    expect(rewriteSources?.('src/index.ts', undefined)).toBe('src/index.ts');
+  });
+
+  it('uses user-provided rewriteSources when given', () => {
+    const customRewrite = (source: string) => `/custom/${source}`;
+    const options = getPluginOptions({ sourcemaps: { rewriteSources: customRewrite } });
+
+    expect(options.sourcemaps?.rewriteSources?.('../../../src/index.ts', undefined)).toBe(
+      '/custom/../../../src/index.ts',
+    );
+  });
+
+  it('always sets metaFramework to nitro', () => {
+    const options = getPluginOptions();
+
+    expect(options._metaOptions?.telemetry?.metaFramework).toBe('nitro');
+  });
+
+  it('passes through sourcemaps.disable', () => {
+    const options = getPluginOptions({ sourcemaps: { disable: 'disable-upload' } });
+
+    expect(options.sourcemaps?.disable).toBe('disable-upload');
+  });
+});
+
+describe('configureSourcemapSettings', () => {
+  it('enables sourcemap generation on the config', () => {
+    const config: NitroConfig = {};
+    const result = configureSourcemapSettings(config);
+
+    expect(config.sourcemap).toBe(true);
+    expect(result.sentryEnabledSourcemaps).toBe(true);
+  });
+
+  it('respects user explicitly disabling sourcemaps and warns', () => {
+    const warnSpy = vi.spyOn(console, 'warn').mockImplementation(() => {});
+    const config: NitroConfig = { sourcemap: false };
+    const result = configureSourcemapSettings(config);
+
+    expect(config.sourcemap).toBe(false);
+    expect(result.sentryEnabledSourcemaps).toBe(false);
+    expect(warnSpy).toHaveBeenCalledWith(expect.stringContaining('explicitly disabled source maps'));
+    warnSpy.mockRestore();
+  });
+
+  it('does not modify experimental config when user disabled sourcemaps', () => {
+    vi.spyOn(console, 'warn').mockImplementation(() => {});
+    const config: NitroConfig = { sourcemap: false };
+    configureSourcemapSettings(config);
+
+    expect(config.experimental).toBeUndefined();
+    vi.restoreAllMocks();
+  });
+
+  it('keeps sourcemap true when user already set it', () => {
+    const config: NitroConfig = { sourcemap: true };
+    const result = configureSourcemapSettings(config);
+
+    expect(config.sourcemap).toBe(true);
+    expect(result.sentryEnabledSourcemaps).toBe(false);
+  });
+
+  it('disables experimental sourcemapMinify', () => {
+    const config: NitroConfig = {};
+    configureSourcemapSettings(config);
+
+    expect(config.experimental?.sourcemapMinify).toBe(false);
+  });
+
+  it('preserves existing experimental config', () => {
+    const config: NitroConfig = {
+      experimental: {
+        sourcemapMinify: undefined,
+      },
+    };
+    configureSourcemapSettings(config);
+
+    expect(config.experimental?.sourcemapMinify).toBe(false);
+  });
+
+  it('skips sourcemap config when sourcemaps.disable is true', () => {
+    const config: NitroConfig = { sourcemap: false };
+    configureSourcemapSettings(config, { sourcemaps: { disable: true } });
+
+    expect(config.sourcemap).toBe(false);
+  });
+
+  it('still configures sourcemaps when sourcemaps.disable is disable-upload', () => {
+    const config: NitroConfig = {};
+    configureSourcemapSettings(config, { sourcemaps: { disable: 'disable-upload' } });
+
+    expect(config.sourcemap).toBe(true);
+  });
+});
+
+describe('setupSentryNitroModule', () => {
+  it('enables tracing', () => {
+    const config: NitroConfig = {};
+    setupSentryNitroModule(config);
+
+    expect(config.tracingChannel).toBe(true);
+  });
+
+  it('adds the sentry module', () => {
+    const config: NitroConfig = {};
+    setupSentryNitroModule(config);
+
+    expect(config.modules).toBeDefined();
+    expect(config.modules?.length).toBe(1);
+  });
+
+  it('still adds module when sourcemaps are disabled', () => {
+    const config: NitroConfig = {};
+    setupSentryNitroModule(config, { sourcemaps: { disable: true } });
+
+    expect(config.modules).toBeDefined();
+    expect(config.modules?.length).toBe(1);
+  });
+});
+
+describe('setupSourceMaps', () => {
+  it('does not register hook in dev mode', () => {
+    const hookFn = vi.fn();
+    const nitro = {
+      options: { dev: true, output: { serverDir: '/output/server' } },
+      hooks: { hook: hookFn },
+    } as any;
+
+    setupSourceMaps(nitro);
+
+    expect(hookFn).not.toHaveBeenCalled();
+  });
+
+  it('does not register hook when sourcemaps.disable is true', () => {
+    const hookFn = vi.fn();
+    const nitro = {
+      options: { dev: false, output: { serverDir: '/output/server' } },
+      hooks: { hook: hookFn },
+    } as any;
+
+    setupSourceMaps(nitro, { sourcemaps: { disable: true } });
+
+    expect(hookFn).not.toHaveBeenCalled();
+  });
+
+  it('does not register hook in nitro-prerender preset', () => {
+    const hookFn = vi.fn();
+    const nitro = {
+      options: { dev: false, preset: 'nitro-prerender', output: { serverDir: '/output/server' } },
+      hooks: { hook: hookFn },
+    } as any;
+
+    setupSourceMaps(nitro);
+
+    expect(hookFn).not.toHaveBeenCalled();
+  });
+
+  it('registers compiled hook in production mode', () => {
+    const hookFn = vi.fn();
+    const nitro = {
+      options: { dev: false, output: { serverDir: '/output/server' } },
+      hooks: { hook: hookFn },
+    } as any;
+
+    setupSourceMaps(nitro);
+
+    expect(hookFn).toHaveBeenCalledWith('compiled', expect.any(Function));
+  });
+
+  it('registers compiled hook with custom options', () => {
+    const hookFn = vi.fn();
+    const nitro = {
+      options: { dev: false, output: { serverDir: '/output/server' } },
+      hooks: { hook: hookFn },
+    } as any;
+
+    setupSourceMaps(nitro, { org: 'my-org', project: 'my-project' });
+
+    expect(hookFn).toHaveBeenCalledWith('compiled', expect.any(Function));
+  });
+});