diff --git a/src/Aspire.Cli/Backchannel/IAuxiliaryBackchannelMonitor.cs b/src/Aspire.Cli/Backchannel/IAuxiliaryBackchannelMonitor.cs
index 36f0a90d257..5ab0d332686 100644
--- a/src/Aspire.Cli/Backchannel/IAuxiliaryBackchannelMonitor.cs
+++ b/src/Aspire.Cli/Backchannel/IAuxiliaryBackchannelMonitor.cs
@@ -31,6 +31,11 @@ internal interface IAuxiliaryBackchannelMonitor
     /// </summary>
     IAppHostAuxiliaryBackchannel? SelectedConnection { get; }
 
+    /// <summary>
+    /// Gets the AppHost path of the currently resolved connection, or <c>null</c> if no connection is available.
+    /// </summary>
+    string? ResolvedAppHostPath => SelectedConnection?.AppHostInfo?.AppHostPath;
+
     /// <summary>
     /// Gets all connections that are within the scope of the specified working directory.
     /// </summary>
diff --git a/src/Aspire.Cli/Mcp/McpResourceToolRefreshService.cs b/src/Aspire.Cli/Mcp/McpResourceToolRefreshService.cs
index e3d3c368333..31e633058d2 100644
--- a/src/Aspire.Cli/Mcp/McpResourceToolRefreshService.cs
+++ b/src/Aspire.Cli/Mcp/McpResourceToolRefreshService.cs
@@ -20,7 +20,7 @@ internal sealed class McpResourceToolRefreshService : IMcpResourceToolRefreshSer
     private McpServer? _server;
     private Dictionary<string, ResourceToolEntry> _resourceToolMap = new(StringComparer.Ordinal);
     private bool _invalidated = true;
-    private string? _selectedAppHostPath;
+    private string? _lastRefreshedAppHostPath;
 
     public McpResourceToolRefreshService(
         IAuxiliaryBackchannelMonitor auxiliaryBackchannelMonitor,
@@ -35,7 +35,7 @@ public bool TryGetResourceToolMap(out IReadOnlyDictionary<string, ResourceToolEn
     {
         lock (_lock)
         {
-            if (_invalidated || _selectedAppHostPath != _auxiliaryBackchannelMonitor.SelectedAppHostPath)
+            if (_invalidated || _lastRefreshedAppHostPath != _auxiliaryBackchannelMonitor.ResolvedAppHostPath)
             {
                 resourceToolMap = null!;
                 return false;
@@ -150,7 +150,7 @@ public async Task SendToolsListChangedNotificationAsync(CancellationToken cancel
             }
 
             _resourceToolMap = refreshedMap;
-            _selectedAppHostPath = selectedAppHostPath;
+            _lastRefreshedAppHostPath = selectedAppHostPath;
             _invalidated = false;
             return (_resourceToolMap, changed);
         }
diff --git a/tests/Aspire.Cli.Tests/Commands/AgentMcpCommandTests.cs b/tests/Aspire.Cli.Tests/Commands/AgentMcpCommandTests.cs
index a4110121431..3bf05fa8694 100644
--- a/tests/Aspire.Cli.Tests/Commands/AgentMcpCommandTests.cs
+++ b/tests/Aspire.Cli.Tests/Commands/AgentMcpCommandTests.cs
@@ -496,6 +496,66 @@ public async Task McpServer_ListTools_DoesNotSendToolsListChangedNotification()
         Assert.Equal(0, notificationCount);
     }
 
+    [Fact]
+    public async Task McpServer_ListTools_CachesResourceToolMap_WhenConnectionUnchanged()
+    {
+        // Arrange - Create a mock backchannel and track how many times GetResourceSnapshotsAsync is called
+        var getResourceSnapshotsCallCount = 0;
+        var mockBackchannel = new TestAppHostAuxiliaryBackchannel
+        {
+            Hash = "test-apphost-hash",
+            IsInScope = true,
+            AppHostInfo = new AppHostInformation
+            {
+                AppHostPath = Path.Combine(_workspace.WorkspaceRoot.FullName, "TestAppHost", "TestAppHost.csproj"),
+                ProcessId = 12345
+            },
+            GetResourceSnapshotsHandler = (ct) =>
+            {
+                Interlocked.Increment(ref getResourceSnapshotsCallCount);
+                return Task.FromResult(new List<ResourceSnapshot>
+                {
+                    new ResourceSnapshot
+                    {
+                        Name = "db-mcp-xyz",
+                        DisplayName = "db-mcp",
+                        ResourceType = "Container",
+                        State = "Running",
+                        McpServer = new ResourceSnapshotMcpServer
+                        {
+                            EndpointUrl = "http://localhost:8080/mcp",
+                            Tools =
+                            [
+                                new Tool
+                                {
+                                    Name = "query_db",
+                                    Description = "Query the database"
+                                }
+                            ]
+                        }
+                    }
+                });
+            }
+        };
+
+        _backchannelMonitor.AddConnection(mockBackchannel.Hash, mockBackchannel.SocketPath, mockBackchannel);
+
+        // Act - Call ListTools twice
+        var tools1 = await _mcpClient.ListToolsAsync(cancellationToken: _cts.Token).DefaultTimeout();
+        var tools2 = await _mcpClient.ListToolsAsync(cancellationToken: _cts.Token).DefaultTimeout();
+
+        // Assert - Both calls return the resource tool
+        Assert.Contains(tools1, t => t.Name == "db_mcp_query_db");
+        Assert.Contains(tools2, t => t.Name == "db_mcp_query_db");
+
+        // The resource tool map should be cached after the first call,
+        // so GetResourceSnapshotsAsync should only be called once (during the first refresh).
+        // Before the fix, TryGetResourceToolMap always returned false due to
+        // SelectedAppHostPath vs SelectedConnection path mismatch, causing every
+        // ListTools call to trigger a full refresh.
+        Assert.Equal(1, getResourceSnapshotsCallCount);
+    }
+
     [Fact]
     public async Task McpServer_CallTool_UnknownTool_ReturnsError()
     {
diff --git a/tests/Aspire.Cli.Tests/TestServices/TestAppHostAuxiliaryBackchannel.cs b/tests/Aspire.Cli.Tests/TestServices/TestAppHostAuxiliaryBackchannel.cs
index 31c7ea06dd8..fe266efc374 100644
--- a/tests/Aspire.Cli.Tests/TestServices/TestAppHostAuxiliaryBackchannel.cs
+++ b/tests/Aspire.Cli.Tests/TestServices/TestAppHostAuxiliaryBackchannel.cs
@@ -46,6 +46,12 @@ internal sealed class TestAppHostAuxiliaryBackchannel : IAppHostAuxiliaryBackcha
     /// </summary>
     public Func<string, string, IReadOnlyDictionary<string, JsonElement>?, CancellationToken, Task<CallToolResult>>? CallResourceMcpToolHandler { get; set; }
 
+    /// <summary>
+    /// Gets or sets the function to call when GetResourceSnapshotsAsync is invoked.
+    /// If null, returns the ResourceSnapshots list.
+    /// </summary>
+    public Func<CancellationToken, Task<List<ResourceSnapshot>>>? GetResourceSnapshotsHandler { get; set; }
+
     public Task<DashboardUrlsState?> GetDashboardUrlsAsync(CancellationToken cancellationToken = default)
     {
         return Task.FromResult(DashboardUrlsState);
@@ -53,6 +59,11 @@ internal sealed class TestAppHostAuxiliaryBackchannel : IAppHostAuxiliaryBackcha
 
     public Task<List<ResourceSnapshot>> GetResourceSnapshotsAsync(CancellationToken cancellationToken = default)
     {
+        if (GetResourceSnapshotsHandler is not null)
+        {
+            return GetResourceSnapshotsHandler(cancellationToken);
+        }
+
         return Task.FromResult(ResourceSnapshots);
     }