diff --git a/node/config.test.ts b/node/config.test.ts
index 1885443a..bbe2945b 100644
--- a/node/config.test.ts
+++ b/node/config.test.ts
@@ -99,6 +99,24 @@ const functions = [
       edge_functions_invalid_config_throw: false,
     },
   },
+  {
+    testName: 'config with correct onError',
+    expectedConfig: { onError: 'bypass' },
+    name: 'func5',
+    source: `
+      export default async () => new Response("Hello from function two")
+      export const config = { onError: "bypass" }
+    `,
+  },
+  {
+    testName: 'config with wrong onError',
+    name: 'func7',
+    source: `
+      export default async () => new Response("Hello from function two")
+      export const config = { onError: "foo" }
+    `,
+    error: /The 'onError' configuration property in edge function at .*/,
+  },
   {
     testName: 'config with `path`',
     expectedConfig: { path: '/home' },
diff --git a/node/config.ts b/node/config.ts
index 60436ddd..5003428a 100644
--- a/node/config.ts
+++ b/node/config.ts
@@ -27,10 +27,19 @@ export const enum Cache {
   Manual = 'manual',
 }
 
+export type OnError = 'fail' | 'bypass' | `/${string}`
+
+export const isValidOnError = (value: unknown): value is OnError => {
+  if (typeof value === 'undefined') return true
+  if (typeof value !== 'string') return false
+  return value === 'fail' || value === 'bypass' || value.startsWith('/')
+}
+
 export interface FunctionConfig {
   cache?: Cache
   path?: string | string[]
   excludedPath?: string | string[]
+  onError?: OnError
 }
 
 const getConfigExtractor = () => {
@@ -89,17 +98,26 @@ export const getFunctionConfig = async (
     log.user(stdout)
   }
 
-  try {
-    const collectorData = await fs.readFile(collector.path, 'utf8')
+  let collectorData: FunctionConfig = {}
 
-    return JSON.parse(collectorData) as FunctionConfig
+  try {
+    const collectorDataJSON = await fs.readFile(collector.path, 'utf8')
+    collectorData = JSON.parse(collectorDataJSON) as FunctionConfig
   } catch {
     handleConfigError(func, ConfigExitCode.UnhandledError, stderr, log, featureFlags)
-
-    return {}
   } finally {
     await collector.cleanup()
   }
+
+  if (!isValidOnError(collectorData.onError)) {
+    throw new BundleError(
+      new Error(
+        `The 'onError' configuration property in edge function at '${func.path}' must be one of 'fail', 'bypass', or a path starting with '/'. Got '${collectorData.onError}'. More on the Edge Functions API at https://ntl.fyi/edge-api.`,
+      ),
+    )
+  }
+
+  return collectorData
 }
 
 const handleConfigError = (
diff --git a/node/manifest.test.ts b/node/manifest.test.ts
index 5bff39bd..b18f38e9 100644
--- a/node/manifest.test.ts
+++ b/node/manifest.test.ts
@@ -3,6 +3,7 @@ import { env } from 'process'
 import { test, expect, vi } from 'vitest'
 
 import { BundleFormat } from './bundle.js'
+import { FunctionConfig } from './config.js'
 import { Declaration } from './declaration.js'
 import { generateManifest } from './manifest.js'
 
@@ -101,6 +102,26 @@ test('Generates a manifest with excluded paths and patterns', () => {
   expect(manifest.bundler_version).toBe(env.npm_package_version as string)
 })
 
+test('Includes failure modes in manifest', () => {
+  const functions = [
+    { name: 'func-1', path: '/path/to/func-1.ts' },
+    { name: 'func-2', path: '/path/to/func-2.ts' },
+  ]
+  const declarations: Declaration[] = [
+    { function: 'func-1', name: 'Display Name', path: '/f1/*' },
+    { function: 'func-2', pattern: '^/f2/.*/?$' },
+  ]
+  const functionConfig: Record<string, FunctionConfig> = {
+    'func-1': {
+      onError: '/custom-error',
+    },
+  }
+  const manifest = generateManifest({ bundles: [], declarations, functions, functionConfig })
+  expect(manifest.function_config).toEqual({
+    'func-1': { excluded_patterns: [], on_error: '/custom-error' },
+  })
+})
+
 test('Excludes functions for which there are function files but no matching config declarations', () => {
   const bundle1 = {
     extension: '.ext2',
diff --git a/node/manifest.ts b/node/manifest.ts
index e3c61ddb..45e49642 100644
--- a/node/manifest.ts
+++ b/node/manifest.ts
@@ -20,6 +20,7 @@ interface Route {
 }
 interface EdgeFunctionConfig {
   excluded_patterns: string[]
+  on_error?: string
 }
 interface Manifest {
   bundler_version: string
@@ -41,13 +42,6 @@ interface GenerateManifestOptions {
   layers?: Layer[]
 }
 
-interface Route {
-  function: string
-  name?: string
-  pattern: string
-  generator?: string
-}
-
 // JavaScript regular expressions are converted to strings with leading and
 // trailing slashes, so any slashes inside the expression itself are escaped
 // as `//`. This function deserializes that back into a single slash, which
@@ -58,7 +52,7 @@ const sanitizeEdgeFunctionConfig = (config: Record<string, EdgeFunctionConfig>):
   const newConfig: Record<string, EdgeFunctionConfig> = {}
 
   for (const [name, functionConfig] of Object.entries(config)) {
-    if (functionConfig.excluded_patterns.length !== 0) {
+    if (functionConfig.excluded_patterns.length !== 0 || functionConfig.on_error) {
       newConfig[name] = functionConfig
     }
   }
@@ -81,13 +75,17 @@ const generateManifest = ({
     functions.map(({ name }) => [name, { excluded_patterns: [] }]),
   )
 
-  for (const [name, { excludedPath }] of Object.entries(functionConfig)) {
+  for (const [name, { excludedPath, onError }] of Object.entries(functionConfig)) {
     if (excludedPath) {
       const paths = Array.isArray(excludedPath) ? excludedPath : [excludedPath]
       const excludedPatterns = paths.map(pathToRegularExpression).map(serializePattern)
 
       manifestFunctionConfig[name].excluded_patterns.push(...excludedPatterns)
     }
+
+    if (onError) {
+      manifestFunctionConfig[name].on_error = onError
+    }
   }
 
   declarations.forEach((declaration) => {
diff --git a/node/validation/manifest/schema.ts b/node/validation/manifest/schema.ts
index 7b36e928..cd66e3aa 100644
--- a/node/validation/manifest/schema.ts
+++ b/node/validation/manifest/schema.ts
@@ -38,6 +38,7 @@ const functionConfigSchema = {
           'excluded_patterns needs to be an array of regex that starts with ^ and ends with $ without any additional slashes before and afterwards',
       },
     },
+    on_error: { type: 'string' },
   },
 }