diff --git a/src/utils/fs.ts b/src/utils/fs.ts
index 852f195a2..c06111810 100644
--- a/src/utils/fs.ts
+++ b/src/utils/fs.ts
@@ -41,34 +41,39 @@ export const safeUnlink = async (path: string) => {
 // filenames within those directories, if at least one of the directories
 // exists. If not, an error is thrown.
 export const listFunctionsDirectories = async function (srcFolders: string[]) {
-  const filenamesByDirectory = await Promise.all(
-    srcFolders.map(async (srcFolder) => {
-      try {
-        const filenames = await listFunctionsDirectory(srcFolder)
-
-        return filenames
-      } catch {
-        return null
-      }
-    }),
+  const filenamesByDirectory = await Promise.allSettled(
+    srcFolders.map((srcFolder) => listFunctionsDirectory(srcFolder)),
   )
-  const validDirectories = filenamesByDirectory.filter(nonNullable)
+  const errorMessages: string[] = []
+  const validDirectories = filenamesByDirectory
+    .map((result) => {
+      if (result.status === 'rejected') {
+        // If the error is about `ENOENT` (FileNotFound) then we only throw later if this happens
+        // for all directories.
+        if (result.reason instanceof Error && (result.reason as NodeJS.ErrnoException).code === 'ENOENT') {
+          return null
+        }
+
+        // In any other error case besides `ENOENT` throw immediately
+        throw result.reason
+      }
+
+      return result.value
+    })
+    .filter(nonNullable)
 
   if (validDirectories.length === 0) {
-    throw new Error(`Functions folder does not exist: ${srcFolders.join(', ')}`)
+    throw new Error(`Functions folders do not exist: ${srcFolders.join(', ')}
+${errorMessages.join('\n')}`)
   }
 
   return validDirectories.flat()
 }
 
-export const listFunctionsDirectory = async function (srcFolder: string) {
-  try {
-    const filenames = await fs.readdir(srcFolder)
+const listFunctionsDirectory = async function (srcFolder: string) {
+  const filenames = await fs.readdir(srcFolder)
 
-    return filenames.map((name) => join(srcFolder, name))
-  } catch {
-    throw new Error(`Functions folder does not exist: ${srcFolder}`)
-  }
+  return filenames.map((name) => join(srcFolder, name))
 }
 
 export const resolveFunctionsDirectories = (input: string | string[]) => {
diff --git a/tests/fixtures/missing-functions-folder/.keep b/tests/fixtures/missing-functions-folder/.keep
new file mode 100644
index 000000000..e69de29bb
diff --git a/tests/main.js b/tests/main.js
index 58a1b5503..ff7dab0f8 100644
--- a/tests/main.js
+++ b/tests/main.js
@@ -823,7 +823,7 @@ testMany(
   ['bundler_default', 'bundler_esbuild', 'bundler_esbuild_zisi', 'bundler_default_nft', 'bundler_nft'],
   async (options, t) => {
     await t.throwsAsync(zipNode(t, 'does-not-exist', { opts: options }), {
-      message: /Functions folder does not exist/,
+      message: /Functions folders do not exist/,
     })
   },
 )
@@ -2700,6 +2700,22 @@ test('listFunction includes in-source config declarations', async (t) => {
   })
 })
 
+test('listFunctionsFiles throws if all function directories do not exist', async (t) => {
+  const error = await t.throwsAsync(
+    async () =>
+      await listFunctionsFiles([
+        join(FIXTURES_DIR, 'missing-functions-folder', 'functions'),
+        join(FIXTURES_DIR, 'missing-functions-folder', 'functions2'),
+      ]),
+  )
+  t.regex(error.message, /Functions folders do not exist: /)
+})
+
+test('listFunctionsFiles does not hide errors that have nothing todo with folder existents', async (t) => {
+  const error = await t.throwsAsync(async () => await listFunctionsFiles([true]))
+  t.notRegex(error.message, /Functions folders do not exist: /)
+})
+
 test('listFunctionsFiles includes in-source config declarations', async (t) => {
   const functions = await listFunctionsFiles(join(FIXTURES_DIR, 'in-source-config', 'functions'), {
     parseISC: true,