diff --git a/packages/plugin-cloud-storage/src/client/createClientUploadHandler.tsx b/packages/plugin-cloud-storage/src/client/createClientUploadHandler.tsx
index a53c16d551..0aab613fe0 100644
--- a/packages/plugin-cloud-storage/src/client/createClientUploadHandler.tsx
+++ b/packages/plugin-cloud-storage/src/client/createClientUploadHandler.tsx
@@ -10,6 +10,7 @@ type ClientUploadHandlerProps<T extends Record<string, unknown>> = {
   collectionSlug: UploadCollectionSlug
   enabled?: boolean
   extra: T
+  prefix?: string
   serverHandlerPath: string
 }
 
@@ -21,6 +22,7 @@ export const createClientUploadHandler = <T extends Record<string, unknown>>({
     collectionSlug: UploadCollectionSlug
     extra: T
     file: File
+    prefix?: string
     serverHandlerPath: string
     serverURL: string
     updateFilename: (value: string) => void
@@ -31,6 +33,7 @@ export const createClientUploadHandler = <T extends Record<string, unknown>>({
     collectionSlug,
     enabled,
     extra,
+    prefix,
     serverHandlerPath,
   }: ClientUploadHandlerProps<T>) {
     const { setUploadHandler } = useUploadHandlers()
@@ -51,6 +54,7 @@ export const createClientUploadHandler = <T extends Record<string, unknown>>({
               collectionSlug,
               extra,
               file,
+              prefix,
               serverHandlerPath,
               serverURL,
               updateFilename,
diff --git a/packages/plugin-cloud-storage/src/utilities/getFilePrefix.ts b/packages/plugin-cloud-storage/src/utilities/getFilePrefix.ts
index fd9778acb5..6e2771f51d 100644
--- a/packages/plugin-cloud-storage/src/utilities/getFilePrefix.ts
+++ b/packages/plugin-cloud-storage/src/utilities/getFilePrefix.ts
@@ -1,14 +1,26 @@
 import type { CollectionConfig, PayloadRequest, UploadConfig } from 'payload'
 
 export async function getFilePrefix({
+  clientUploadContext,
   collection,
   filename,
   req,
 }: {
+  clientUploadContext?: unknown
   collection: CollectionConfig
   filename: string
   req: PayloadRequest
 }): Promise<string> {
+  // Prioritize from clientUploadContext if there is:
+  if (
+    clientUploadContext &&
+    typeof clientUploadContext === 'object' &&
+    'prefix' in clientUploadContext &&
+    typeof clientUploadContext.prefix === 'string'
+  ) {
+    return clientUploadContext.prefix
+  }
+
   const imageSizes = (collection?.upload as UploadConfig)?.imageSizes || []
 
   const files = await req.payload.find({
diff --git a/packages/plugin-cloud-storage/src/utilities/initClientUploads.ts b/packages/plugin-cloud-storage/src/utilities/initClientUploads.ts
index 316995c380..6b8b454e73 100644
--- a/packages/plugin-cloud-storage/src/utilities/initClientUploads.ts
+++ b/packages/plugin-cloud-storage/src/utilities/initClientUploads.ts
@@ -63,11 +63,23 @@ export const initClientUploads = <ExtraProps extends Record<string, unknown>, T>
   for (const collectionSlug in collections) {
     const collection = collections[collectionSlug]
 
+    let prefix: string | undefined
+
+    if (
+      collection &&
+      typeof collection === 'object' &&
+      'prefix' in collection &&
+      typeof collection.prefix === 'string'
+    ) {
+      prefix = collection.prefix
+    }
+
     config.admin.components.providers.push({
       clientProps: {
         collectionSlug,
         enabled,
         extra: extraClientHandlerProps ? extraClientHandlerProps(collection) : undefined,
+        prefix,
         serverHandlerPath,
       },
       path: clientHandler,
diff --git a/packages/storage-azure/src/client/AzureClientUploadHandler.ts b/packages/storage-azure/src/client/AzureClientUploadHandler.ts
index c61251fea6..f615962dc6 100644
--- a/packages/storage-azure/src/client/AzureClientUploadHandler.ts
+++ b/packages/storage-azure/src/client/AzureClientUploadHandler.ts
@@ -2,7 +2,7 @@
 import { createClientUploadHandler } from '@payloadcms/plugin-cloud-storage/client'
 
 export const AzureClientUploadHandler = createClientUploadHandler({
-  handler: async ({ apiRoute, collectionSlug, file, serverHandlerPath, serverURL }) => {
+  handler: async ({ apiRoute, collectionSlug, file, prefix, serverHandlerPath, serverURL }) => {
     const response = await fetch(`${serverURL}${apiRoute}${serverHandlerPath}`, {
       body: JSON.stringify({
         collectionSlug,
@@ -25,5 +25,7 @@ export const AzureClientUploadHandler = createClientUploadHandler({
       },
       method: 'PUT',
     })
+
+    return { prefix }
   },
 })
diff --git a/packages/storage-azure/src/staticHandler.ts b/packages/storage-azure/src/staticHandler.ts
index 0dcc888b7d..58ea821120 100644
--- a/packages/storage-azure/src/staticHandler.ts
+++ b/packages/storage-azure/src/staticHandler.ts
@@ -13,9 +13,9 @@ interface Args {
 }
 
 export const getHandler = ({ collection, getStorageClient }: Args): StaticHandler => {
-  return async (req, { params: { filename } }) => {
+  return async (req, { params: { clientUploadContext, filename } }) => {
     try {
-      const prefix = await getFilePrefix({ collection, filename, req })
+      const prefix = await getFilePrefix({ clientUploadContext, collection, filename, req })
       const blockBlobClient = getStorageClient().getBlockBlobClient(
         path.posix.join(prefix, filename),
       )
diff --git a/packages/storage-gcs/src/client/GcsClientUploadHandler.ts b/packages/storage-gcs/src/client/GcsClientUploadHandler.ts
index 549c5a3c17..84b8a41320 100644
--- a/packages/storage-gcs/src/client/GcsClientUploadHandler.ts
+++ b/packages/storage-gcs/src/client/GcsClientUploadHandler.ts
@@ -2,7 +2,7 @@
 import { createClientUploadHandler } from '@payloadcms/plugin-cloud-storage/client'
 
 export const GcsClientUploadHandler = createClientUploadHandler({
-  handler: async ({ apiRoute, collectionSlug, file, serverHandlerPath, serverURL }) => {
+  handler: async ({ apiRoute, collectionSlug, file, prefix, serverHandlerPath, serverURL }) => {
     const response = await fetch(`${serverURL}${apiRoute}${serverHandlerPath}`, {
       body: JSON.stringify({
         collectionSlug,
@@ -20,5 +20,9 @@ export const GcsClientUploadHandler = createClientUploadHandler({
       headers: { 'Content-Length': file.size.toString(), 'Content-Type': file.type },
       method: 'PUT',
     })
+
+    return {
+      prefix,
+    }
   },
 })
diff --git a/packages/storage-gcs/src/staticHandler.ts b/packages/storage-gcs/src/staticHandler.ts
index 0103c9d700..f6828fe834 100644
--- a/packages/storage-gcs/src/staticHandler.ts
+++ b/packages/storage-gcs/src/staticHandler.ts
@@ -12,9 +12,9 @@ interface Args {
 }
 
 export const getHandler = ({ bucket, collection, getStorageClient }: Args): StaticHandler => {
-  return async (req, { params: { filename } }) => {
+  return async (req, { params: { clientUploadContext, filename } }) => {
     try {
-      const prefix = await getFilePrefix({ collection, filename, req })
+      const prefix = await getFilePrefix({ clientUploadContext, collection, filename, req })
       const file = getStorageClient().bucket(bucket).file(path.posix.join(prefix, filename))
 
       const [metadata] = await file.getMetadata()
diff --git a/packages/storage-s3/src/client/S3ClientUploadHandler.ts b/packages/storage-s3/src/client/S3ClientUploadHandler.ts
index 7f1748a89d..c4dc148aab 100644
--- a/packages/storage-s3/src/client/S3ClientUploadHandler.ts
+++ b/packages/storage-s3/src/client/S3ClientUploadHandler.ts
@@ -2,7 +2,7 @@
 import { createClientUploadHandler } from '@payloadcms/plugin-cloud-storage/client'
 
 export const S3ClientUploadHandler = createClientUploadHandler({
-  handler: async ({ apiRoute, collectionSlug, file, serverHandlerPath, serverURL }) => {
+  handler: async ({ apiRoute, collectionSlug, file, prefix, serverHandlerPath, serverURL }) => {
     const response = await fetch(`${serverURL}${apiRoute}${serverHandlerPath}`, {
       body: JSON.stringify({
         collectionSlug,
@@ -20,5 +20,7 @@ export const S3ClientUploadHandler = createClientUploadHandler({
       headers: { 'Content-Length': file.size.toString(), 'Content-Type': file.type },
       method: 'PUT',
     })
+
+    return { prefix }
   },
 })
diff --git a/packages/storage-s3/src/staticHandler.ts b/packages/storage-s3/src/staticHandler.ts
index 7b903e7b52..056ed7678d 100644
--- a/packages/storage-s3/src/staticHandler.ts
+++ b/packages/storage-s3/src/staticHandler.ts
@@ -35,9 +35,9 @@ const streamToBuffer = async (readableStream: any) => {
 }
 
 export const getHandler = ({ bucket, collection, getStorageClient }: Args): StaticHandler => {
-  return async (req, { params: { filename } }) => {
+  return async (req, { params: { clientUploadContext, filename } }) => {
     try {
-      const prefix = await getFilePrefix({ collection, filename, req })
+      const prefix = await getFilePrefix({ clientUploadContext, collection, filename, req })
 
       const key = path.posix.join(prefix, filename)