diff --git a/src/Runner.Common/Constants.cs b/src/Runner.Common/Constants.cs
index 8533e931a..4f8694d53 100644
--- a/src/Runner.Common/Constants.cs
+++ b/src/Runner.Common/Constants.cs
@@ -90,7 +90,7 @@ namespace GitHub.Runner.Common
                     public static readonly string Labels = "labels";
                     public static readonly string MonitorSocketAddress = "monitorsocketaddress";
                     public static readonly string Name = "name";
-                    public static readonly string Pool = "pool";
+                    public static readonly string RunnerGroup = "runnergroup";
                     public static readonly string StartupType = "startuptype";
                     public static readonly string Url = "url";
                     public static readonly string UserName = "username";
diff --git a/src/Runner.Listener/CommandSettings.cs b/src/Runner.Listener/CommandSettings.cs
index 0d80c1d5e..364962610 100644
--- a/src/Runner.Listener/CommandSettings.cs
+++ b/src/Runner.Listener/CommandSettings.cs
@@ -42,7 +42,7 @@ namespace GitHub.Runner.Listener
             Constants.Runner.CommandLine.Args.Labels,
             Constants.Runner.CommandLine.Args.MonitorSocketAddress,
             Constants.Runner.CommandLine.Args.Name,
-            Constants.Runner.CommandLine.Args.Pool,
+            Constants.Runner.CommandLine.Args.RunnerGroup,
             Constants.Runner.CommandLine.Args.StartupType,
             Constants.Runner.CommandLine.Args.Token,
             Constants.Runner.CommandLine.Args.Url,
@@ -169,6 +169,15 @@ namespace GitHub.Runner.Listener
                 validator: Validators.NonEmptyValidator);
         }
 
+        public string GetRunnerGroupName(string defaultPoolName = null)
+        {
+            return GetArgOrPrompt(
+                name: Constants.Runner.CommandLine.Args.RunnerGroup,
+                description: "Enter the name of the runner group to add this runner to:",
+                defaultValue: defaultPoolName ?? "default",
+                validator: Validators.NonEmptyValidator);
+        }
+
         public string GetToken()
         {
             return GetArgOrPrompt(
diff --git a/src/Runner.Listener/Configuration/ConfigurationManager.cs b/src/Runner.Listener/Configuration/ConfigurationManager.cs
index ce0863e1a..8e499adc7 100644
--- a/src/Runner.Listener/Configuration/ConfigurationManager.cs
+++ b/src/Runner.Listener/Configuration/ConfigurationManager.cs
@@ -159,17 +159,34 @@ namespace GitHub.Runner.Listener.Configuration
 
             _term.WriteSection("Runner Registration");
 
-            //Get all the agent pools, and select the first private pool
+            // If we have more than one runner group available, allow the user to specify which one to be added into
+            string poolName = null;
+            TaskAgentPool agentPool = null;
             List<TaskAgentPool> agentPools = await _runnerServer.GetAgentPoolsAsync();
-            TaskAgentPool agentPool = agentPools?.Where(x => x.IsHosted == false).FirstOrDefault();
+            TaskAgentPool defaultPool = agentPools?.Where(x => x.IsInternal).FirstOrDefault();
 
-            if (agentPool == null)
+            if (agentPools?.Where(x => !x.IsHosted).Count() > 1)
             {
-                throw new TaskAgentPoolNotFoundException($"Could not find any private pool. Contact support.");
+                poolName = command.GetRunnerGroupName(defaultPool?.Name);
+                _term.WriteLine();
+                agentPool = agentPools.Where(x => string.Equals(poolName, x.Name, StringComparison.OrdinalIgnoreCase) && !x.IsHosted).FirstOrDefault();
             }
             else
             {
-                Trace.Info("Found a private pool with id {1} and name {2}", agentPool.Id, agentPool.Name);
+                agentPool = defaultPool;
+            }
+
+            if (agentPool == null && poolName == null)
+            {
+                throw new TaskAgentPoolNotFoundException($"Could not find any self-hosted runner groups. Contact support.");
+            }
+            else if (agentPool == null && poolName != null)
+            {
+                throw new TaskAgentPoolNotFoundException($"Could not find any self-hosted runner group named \"{poolName}\".");
+            }
+            else
+            {
+                Trace.Info("Found a self-hosted runner group with id {1} and name {2}", agentPool.Id, agentPool.Name);
                 runnerSettings.PoolId = agentPool.Id;
                 runnerSettings.PoolName = agentPool.Name;
             }
diff --git a/src/Sdk/DTWebApi/WebApi/TaskAgentPoolReference.cs b/src/Sdk/DTWebApi/WebApi/TaskAgentPoolReference.cs
index bbef3809f..714860c1d 100644
--- a/src/Sdk/DTWebApi/WebApi/TaskAgentPoolReference.cs
+++ b/src/Sdk/DTWebApi/WebApi/TaskAgentPoolReference.cs
@@ -29,6 +29,7 @@ namespace GitHub.DistributedTask.WebApi
             this.PoolType = referenceToBeCloned.PoolType;
             this.Size = referenceToBeCloned.Size;
             this.IsLegacy = referenceToBeCloned.IsLegacy;
+            this.IsInternal = referenceToBeCloned.IsInternal;
         }
 
         public TaskAgentPoolReference Clone()
@@ -67,6 +68,16 @@ namespace GitHub.DistributedTask.WebApi
             set;
         }
 
+        /// <summary>
+        /// Gets or sets a value indicating whether or not this pool is internal and can't be modified by users
+        /// </summary>
+        [DataMember]
+        public bool IsInternal
+        {
+            get;
+            set;
+        }
+
         /// <summary>
         /// Gets or sets the type of the pool
         /// </summary>
diff --git a/src/Test/L0/Listener/Configuration/ConfigurationManagerL0.cs b/src/Test/L0/Listener/Configuration/ConfigurationManagerL0.cs
index 9cf3ad5ad..706a11cd7 100644
--- a/src/Test/L0/Listener/Configuration/ConfigurationManagerL0.cs
+++ b/src/Test/L0/Listener/Configuration/ConfigurationManagerL0.cs
@@ -39,10 +39,12 @@ namespace GitHub.Runner.Common.Tests.Listener.Configuration
         private string _expectedToken = "expectedToken";
         private string _expectedServerUrl = "https://codedev.ms";
         private string _expectedAgentName = "expectedAgentName";
-        private string _expectedPoolName = "poolName";
+        private string _defaultRunnerGroupName = "defaultRunnerGroup";
+        private string _secondRunnerGroupName = "secondRunnerGroup";
         private string _expectedAuthType = "pat";
         private string _expectedWorkFolder = "_work";
-        private int _expectedPoolId = 1;
+        private int _defaultRunnerGroupId = 1;
+        private int _secondRunnerGroupId = 2;
         private RSACryptoServiceProvider rsa = null;
         private RunnerSettings _configMgrAgentSettings = new RunnerSettings();
 
@@ -97,7 +99,7 @@ namespace GitHub.Runner.Common.Tests.Listener.Configuration
             _serviceControlManager.Setup(x => x.GenerateScripts(It.IsAny<RunnerSettings>()));
 #endif
 
-            var expectedPools = new List<TaskAgentPool>() { new TaskAgentPool(_expectedPoolName) { Id = _expectedPoolId } };
+            var expectedPools = new List<TaskAgentPool>() { new TaskAgentPool(_defaultRunnerGroupName) { Id = _defaultRunnerGroupId, IsInternal = true }, new TaskAgentPool(_secondRunnerGroupName) { Id = _secondRunnerGroupId } };
             _runnerServer.Setup(x => x.GetAgentPoolsAsync(It.IsAny<string>(), It.IsAny<TaskAgentPoolType>())).Returns(Task.FromResult(expectedPools));
 
             var expectedAgents = new List<TaskAgent>();
@@ -155,7 +157,7 @@ namespace GitHub.Runner.Common.Tests.Listener.Configuration
                        "configure",                
                        "--url", _expectedServerUrl,
                        "--name", _expectedAgentName,
-                       "--pool", _expectedPoolName,
+                       "--runnergroup", _secondRunnerGroupName,
                        "--work", _expectedWorkFolder,
                        "--auth", _expectedAuthType,
                        "--token", _expectedToken,
@@ -175,7 +177,7 @@ namespace GitHub.Runner.Common.Tests.Listener.Configuration
                 Assert.NotNull(s);
                 Assert.True(s.ServerUrl.Equals(_expectedServerUrl));
                 Assert.True(s.AgentName.Equals(_expectedAgentName));
-                Assert.True(s.PoolId.Equals(_expectedPoolId));
+                Assert.True(s.PoolId.Equals(_secondRunnerGroupId));
                 Assert.True(s.WorkFolder.Equals(_expectedWorkFolder));
 
                 // validate GetAgentPoolsAsync gets called twice with automation pool type