diff --git a/src/System.Management.Automation/engine/CommandCompletion/CompletionCompleters.cs b/src/System.Management.Automation/engine/CommandCompletion/CompletionCompleters.cs
index 415471362c..11fae48b2f 100644
--- a/src/System.Management.Automation/engine/CommandCompletion/CompletionCompleters.cs
+++ b/src/System.Management.Automation/engine/CommandCompletion/CompletionCompleters.cs
@@ -1993,16 +1993,27 @@ namespace System.Management.Automation
             CompletionContext context,
             Dictionary<string, AstParameterArgumentPair> boundArguments = null)
         {
-            if (string.IsNullOrEmpty(commandName))
+            string parameterName = parameter.Name;
+
+            // Fall back to the commandAst command name if a command name is not found. This can be caused by a script block or AST with the matching function definition being passed to CompleteInput
+            // This allows for editors and other tools using CompleteInput with Script/AST definations to get values from RegisteredArgumentCompleters to better match the console experience.
+            // See issue https://github.com/PowerShell/PowerShell/issues/10567
+            string actualCommandName = string.IsNullOrEmpty(commandName)
+                        ? commandAst.GetCommandName()
+                        : commandName;
+
+            if (string.IsNullOrEmpty(actualCommandName))
             {
                 return;
             }
 
-            var parameterName = parameter.Name;
-            var customCompleter = GetCustomArgumentCompleter(
-                    "CustomArgumentCompleters",
-                    new[] { commandName + ":" + parameterName, parameterName },
-                    context);
+            string parameterFullName = $"{actualCommandName}:{parameterName}";
+
+            ScriptBlock customCompleter = GetCustomArgumentCompleter(
+                "CustomArgumentCompleters",
+                new[] { parameterFullName, parameterName },
+                context);
+
             if (customCompleter != null)
             {
                 if (InvokeScriptArgumentCompleter(
diff --git a/test/powershell/Host/TabCompletion/TabCompletion.Tests.ps1 b/test/powershell/Host/TabCompletion/TabCompletion.Tests.ps1
index 7285798830..de231bd8e8 100644
--- a/test/powershell/Host/TabCompletion/TabCompletion.Tests.ps1
+++ b/test/powershell/Host/TabCompletion/TabCompletion.Tests.ps1
@@ -836,6 +836,32 @@ Describe "TabCompletion" -Tags CI {
             $res.CompletionMatches[1].CompletionText | Should -BeExactly 'dog'
         }
 
+        It "Tab completion for ArgumentCompleter when AST is passed to CompleteInput" {
+            $scriptBl = {
+                function Test-Completion {
+                    param (
+                        [String]$TestVal
+                    )
+                }
+                [scriptblock]$completer = {
+                    param($commandName, $parameterName, $wordToComplete, $commandAst, $fakeBoundParameters)
+
+                    @('Val1', 'Val2')
+                }
+                Register-ArgumentCompleter -CommandName Test-Completion -ParameterName TestVal -ScriptBlock $completer
+            }
+            $pwsh = [PowerShell]::Create()
+            $pwsh.AddScript($scriptBl)
+            $pwsh.Invoke()
+
+            $completeInput_Input = $scriptBl.ToString()
+            $completeInput_Input += "`nTest-Completion -TestVal "
+            $res = [System.Management.Automation.CommandCompletion]::CompleteInput($completeInput_Input, $completeInput_Input.Length, $null, $pwsh)
+            $res.CompletionMatches | Should -HaveCount 2
+            $res.CompletionMatches[0].CompletionText | Should -BeExactly 'Val1'
+            $res.CompletionMatches[1].CompletionText | Should -BeExactly 'Val2'
+        }
+
         It "Tab completion for enum type parameter of a custom function" {
             function baz ([consolecolor]$name, [ValidateSet('cat','dog')]$p){}
             $inputStr = "baz -name "