diff --git a/test/powershell/Modules/Microsoft.PowerShell.Utility/WebCmdlets.Tests.ps1 b/test/powershell/Modules/Microsoft.PowerShell.Utility/WebCmdlets.Tests.ps1
index 2b2968ea3da..79aaf2f1033 100644
--- a/test/powershell/Modules/Microsoft.PowerShell.Utility/WebCmdlets.Tests.ps1
+++ b/test/powershell/Modules/Microsoft.PowerShell.Utility/WebCmdlets.Tests.ps1
@@ -2145,6 +2145,16 @@ Describe "Invoke-WebRequest tests" -Tags "Feature", "RequireAdminOnWindows" {
             $jsonError.error | Should -BeExactly 'Error: HTTP - 400 occurred.'
         }
 
+        It "Invoke-WebRequest can retry - specified number of times following Retry-After header - error 429" {
+
+            $uri = Get-WebListenerUrl -Test 'Retry' -Query @{ sessionid = (New-Guid).Guid; failureCode = 429; failureCount = 2; retryAfter = 2 }
+            $verboseFile = Join-Path $TestDrive -ChildPath verbose.txt
+            $result = Invoke-WebRequest -Uri $uri -MaximumRetryCount 2 -RetryIntervalSec 1 -Verbose 4>>$verboseFile
+
+            $result.StatusCode | Should -Be "200"
+            $verboseFile | Should -FileContentMatch "Retrying after interval of 2 seconds. Status code for previous attempt: TooManyRequests"
+        }
+
         It "Invoke-WebRequest can retry with POST" {
 
             $uri = Get-WebListenerUrl -Test 'Retry'
@@ -4036,6 +4046,15 @@ Describe "Invoke-RestMethod tests" -Tags "Feature", "RequireAdminOnWindows" {
             $result.output.sessionId | Should -BeExactly $sessionId
         }
 
+        It "Invoke-RestMethod can retry - specified number of times following Retry-After header - error 429" {
+
+            $uri = Get-WebListenerUrl -Test 'Retry' -Query @{ sessionid = (New-Guid).Guid; failureCode = 429; failureCount = 2; retryAfter = 2 }
+            $verboseFile = Join-Path $TestDrive -ChildPath verbose.txt
+            $result = Invoke-RestMethod -Uri $uri -MaximumRetryCount 2 -RetryIntervalSec 1 -Verbose 4>>$verboseFile
+
+            $verboseFile | Should -FileContentMatch "Retrying after interval of 2 seconds. Status code for previous attempt: TooManyRequests"
+        }
+
         It "Invoke-RestMethod can retry with POST" {
 
             $uri = Get-WebListenerUrl -Test 'Retry'
diff --git a/test/tools/WebListener/Controllers/RetryController.cs b/test/tools/WebListener/Controllers/RetryController.cs
index f9f93bae4c0..bdb70ff0f12 100644
--- a/test/tools/WebListener/Controllers/RetryController.cs
+++ b/test/tools/WebListener/Controllers/RetryController.cs
@@ -9,6 +9,7 @@
 using System.Net;
 using System.Threading;
 using System.Threading.Tasks;
+using Microsoft.AspNetCore.Http;
 using Microsoft.AspNetCore.Http.Extensions;
 using Microsoft.AspNetCore.Mvc;
 using Microsoft.Extensions.Primitives;
@@ -21,10 +22,15 @@ public class RetryController : Controller
         // Dictionary for sessionId as key and failureCode, failureCount and failureResponsesSent as the value.
         private static Dictionary<string, Tuple<int, int, int>> retryInfo;
 
-        public JsonResult Retry(string sessionId, int failureCode, int failureCount)
+        public JsonResult Retry(string sessionId, int failureCode, int failureCount, int retryAfter = 0)
         {
             retryInfo ??= new Dictionary<string, Tuple<int, int, int>>();
 
+            if (failureCode == 429 && retryAfter > 0)
+            {
+                Response.Headers.Append("Retry-After", $"{retryAfter}");
+            }
+
             if (retryInfo.TryGetValue(sessionId, out Tuple<int, int, int> retry))
             {
                 // if failureResponsesSent is less than failureCount