diff --git a/src/Microsoft.Android.Run/Microsoft.Android.Run.csproj b/src/Microsoft.Android.Run/Microsoft.Android.Run.csproj
index de8fb6bf5c8..4d83d44e3c2 100644
--- a/src/Microsoft.Android.Run/Microsoft.Android.Run.csproj
+++ b/src/Microsoft.Android.Run/Microsoft.Android.Run.csproj
@@ -11,6 +11,7 @@
     <Nullable>enable</Nullable>
     <DebugType>portable</DebugType>
     <RollForward>Major</RollForward>
+    <StartupHookSupport>false</StartupHookSupport>
   </PropertyGroup>
 
   <ItemGroup>
diff --git a/src/Xamarin.Android.Build.Tasks/Microsoft.Android.Sdk/targets/Microsoft.Android.Sdk.After.targets b/src/Xamarin.Android.Build.Tasks/Microsoft.Android.Sdk/targets/Microsoft.Android.Sdk.After.targets
index 9cb93fb2e06..01a64d12687 100644
--- a/src/Xamarin.Android.Build.Tasks/Microsoft.Android.Sdk/targets/Microsoft.Android.Sdk.After.targets
+++ b/src/Xamarin.Android.Build.Tasks/Microsoft.Android.Sdk/targets/Microsoft.Android.Sdk.After.targets
@@ -33,4 +33,5 @@ This file is imported *after* the Microsoft.NET.Sdk/Sdk.targets.
   <Import Project="Microsoft.Android.Sdk.Publish.targets" />
   <Import Project="Microsoft.Android.Sdk.RuntimeConfig.targets" />
   <Import Project="Microsoft.Android.Sdk.Tooling.targets" />
+  <Import Project="Microsoft.Android.Sdk.HotReload.targets" Condition=" '$(AndroidApplication)' == 'true' " />
 </Project>
diff --git a/src/Xamarin.Android.Build.Tasks/Microsoft.Android.Sdk/targets/Microsoft.Android.Sdk.Application.targets b/src/Xamarin.Android.Build.Tasks/Microsoft.Android.Sdk/targets/Microsoft.Android.Sdk.Application.targets
index d6efbf7b5ee..3bd96d38fbe 100644
--- a/src/Xamarin.Android.Build.Tasks/Microsoft.Android.Sdk/targets/Microsoft.Android.Sdk.Application.targets
+++ b/src/Xamarin.Android.Build.Tasks/Microsoft.Android.Sdk/targets/Microsoft.Android.Sdk.Application.targets
@@ -25,6 +25,7 @@ This file contains targets specific for Android application projects.
     <_AndroidComputeRunArgumentsDependsOn Condition=" '$(_AndroidComputeRunArgumentsDependsOn)' == '' ">
       _ResolveMonoAndroidSdks;
       _GetAndroidPackageName;
+      _AndroidAdbToolPath;
     </_AndroidComputeRunArgumentsDependsOn>
   </PropertyGroup>
 
@@ -49,6 +50,15 @@ This file contains targets specific for Android application projects.
     </GetAvailableAndroidDevices>
   </Target>
 
+  <Target Name="_AndroidAdbToolPath">
+    <PropertyGroup>
+      <_AdbToolPath>$(AdbToolExe)</_AdbToolPath>
+      <_AdbToolPath Condition=" '$(_AdbToolPath)' == '' and $([MSBuild]::IsOSPlatform('windows')) ">adb.exe</_AdbToolPath>
+      <_AdbToolPath Condition=" '$(_AdbToolPath)' == '' and !$([MSBuild]::IsOSPlatform('windows')) ">adb</_AdbToolPath>
+      <_AdbToolPath>$([System.IO.Path]::Combine ('$(AdbToolPath)', '$(_AdbToolPath)'))</_AdbToolPath>
+    </PropertyGroup>
+  </Target>
+
   <Target Name="_AndroidComputeRunArguments"
       BeforeTargets="ComputeRunArguments"
       DependsOnTargets="$(_AndroidComputeRunArgumentsDependsOn)">
@@ -58,10 +68,6 @@ This file contains targets specific for Android application projects.
       <Output TaskParameter="ActivityName" PropertyName="AndroidLaunchActivity" />
     </GetAndroidActivityName>
     <PropertyGroup>
-      <_AdbToolPath>$(AdbToolExe)</_AdbToolPath>
-      <_AdbToolPath Condition=" '$(_AdbToolPath)' == '' and $([MSBuild]::IsOSPlatform('windows')) ">adb.exe</_AdbToolPath>
-      <_AdbToolPath Condition=" '$(_AdbToolPath)' == '' and !$([MSBuild]::IsOSPlatform('windows')) ">adb</_AdbToolPath>
-      <_AdbToolPath>$([System.IO.Path]::Combine ('$(AdbToolPath)', '$(_AdbToolPath)'))</_AdbToolPath>
       <RunWorkingDirectory>$(MSBuildProjectDirectory)</RunWorkingDirectory>
     </PropertyGroup>
     <!-- By default, use `Microsoft.Android.Run` tool to stream logcat and handle Ctrl+C -->
diff --git a/src/Xamarin.Android.Build.Tasks/Microsoft.Android.Sdk/targets/Microsoft.Android.Sdk.AssemblyResolution.targets b/src/Xamarin.Android.Build.Tasks/Microsoft.Android.Sdk/targets/Microsoft.Android.Sdk.AssemblyResolution.targets
index b1717d2b0fe..4ba95ac50e2 100644
--- a/src/Xamarin.Android.Build.Tasks/Microsoft.Android.Sdk/targets/Microsoft.Android.Sdk.AssemblyResolution.targets
+++ b/src/Xamarin.Android.Build.Tasks/Microsoft.Android.Sdk/targets/Microsoft.Android.Sdk.AssemblyResolution.targets
@@ -74,7 +74,7 @@ _ResolveAssemblies MSBuild target.
     </ItemGroup>
   </Target>
 
-  <Target Name="_ResolveAssemblies">
+  <Target Name="_ResolveAssemblies" DependsOnTargets="_AndroidConfigureHotReloadEnvironment">
     <ItemGroup>
       <_RIDs Include="$(RuntimeIdentifier)"  Condition=" '$(RuntimeIdentifiers)' == '' " />
       <_RIDs Include="$(RuntimeIdentifiers)" Condition=" '$(RuntimeIdentifiers)' != '' " />
@@ -120,6 +120,7 @@ _ResolveAssemblies MSBuild target.
     </ProcessRuntimePackLibraryDirectories>
 
     <ItemGroup>
+      <ResolvedFileToPublish Include="$(_AndroidHotReloadAgentAssemblyPath)" Condition="Exists('$(_AndroidHotReloadAgentAssemblyPath)')" RuntimeIdentifier="%(_RIDs.Identity)" />
       <ResolvedFileToPublish Remove="@(_NativeLibraryToRemove)" />
     </ItemGroup>
 
diff --git a/src/Xamarin.Android.Build.Tasks/Microsoft.Android.Sdk/targets/Microsoft.Android.Sdk.BuildOrder.targets b/src/Xamarin.Android.Build.Tasks/Microsoft.Android.Sdk/targets/Microsoft.Android.Sdk.BuildOrder.targets
index 039bc54f78a..9bb66ab4073 100644
--- a/src/Xamarin.Android.Build.Tasks/Microsoft.Android.Sdk/targets/Microsoft.Android.Sdk.BuildOrder.targets
+++ b/src/Xamarin.Android.Build.Tasks/Microsoft.Android.Sdk/targets/Microsoft.Android.Sdk.BuildOrder.targets
@@ -99,6 +99,7 @@ properties that determine build ordering.
       SignAndroidPackage;
       _DeployApk;
       _DeployAppBundle;
+      _AndroidConfigureAdbReverse;
     </InstallDependsOnTargets>
     <UninstallDependsOnTargets>
       AndroidPrepareForBuild;
@@ -127,12 +128,16 @@ properties that determine build ordering.
     <!-- This should function similar to SignAndroidPackage inside VS plus also deploy -->
     <DeployToDeviceDependsOnTargets Condition=" '$(_AndroidFastDeploymentSupported)' == 'true' ">
       $(_MinimalSignAndroidPackageDependsOn);
+      _GenerateEnvironmentFiles;
       _Upload;
+      _AndroidConfigureAdbReverse;
     </DeployToDeviceDependsOnTargets>
     <DeployToDeviceDependsOnTargets Condition=" '$(_AndroidFastDeploymentSupported)' != 'true' ">
       $(_MinimalSignAndroidPackageDependsOn);
+      _GenerateEnvironmentFiles;
       _DeployApk;
       _DeployAppBundle;
+      _AndroidConfigureAdbReverse;
     </DeployToDeviceDependsOnTargets>
   </PropertyGroup>
 
diff --git a/src/Xamarin.Android.Build.Tasks/Microsoft.Android.Sdk/targets/Microsoft.Android.Sdk.HotReload.targets b/src/Xamarin.Android.Build.Tasks/Microsoft.Android.Sdk/targets/Microsoft.Android.Sdk.HotReload.targets
new file mode 100644
index 00000000000..0e887dcf6c6
--- /dev/null
+++ b/src/Xamarin.Android.Build.Tasks/Microsoft.Android.Sdk/targets/Microsoft.Android.Sdk.HotReload.targets
@@ -0,0 +1,84 @@
+<!--
+***********************************************************************************************
+Microsoft.Android.Sdk.HotReload.targets
+
+This file contains targets for Hot Reload support in .NET for Android.
+These targets are invoked by dotnet-watch when Hot Reload starts.
+
+dotnet-watch passes environment variables via @(RuntimeEnvironmentVariable) items:
+- DOTNET_STARTUP_HOOKS: Path to Microsoft.Extensions.DotNetDeltaApplier.dll
+- DOTNET_WATCH_HOTRELOAD_WEBSOCKET_ENDPOINT: WebSocket endpoint URL for hot reload communication
+
+The environment variables are written to the app by the _GenerateEnvironmentFiles target
+in Xamarin.Android.Common.targets, which includes @(RuntimeEnvironmentVariable) items.
+
+See: https://github.com/dotnet/sdk/issues/52492
+See: https://github.com/dotnet/sdk/pull/52581
+
+***********************************************************************************************
+-->
+
+<Project>
+
+  <!--
+    _AndroidConfigureHotReloadEnvironment:
+    Configures Hot Reload when dotnet-watch passes environment variables via @(RuntimeEnvironmentVariable).
+    - Adds the Hot Reload agent DLL as a reference so it gets deployed
+    - Updates DOTNET_STARTUP_HOOKS to use just the assembly name (not the full path)
+    - Sets up STARTUP_HOOKS via RuntimeHostConfigurationOption for MonoVM
+  -->
+  <Target Name="_AndroidConfigureHotReloadEnvironment"
+          Condition=" '@(RuntimeEnvironmentVariable)' != '' ">
+
+    <!-- Extract the startup hooks value from @(RuntimeEnvironmentVariable) -->
+    <PropertyGroup>
+      <_AndroidHotReloadAgentAssemblyPath>@(RuntimeEnvironmentVariable->WithMetadataValue('Identity', 'DOTNET_STARTUP_HOOKS')->'%(Value)'->Exists())</_AndroidHotReloadAgentAssemblyPath>
+    </PropertyGroup>
+
+    <!-- Extract just the assembly name for STARTUP_HOOKS config -->
+    <PropertyGroup Condition=" '$(_AndroidHotReloadAgentAssemblyPath)' != '' ">
+      <_AndroidHotReloadAgentAssemblyName>$([System.IO.Path]::GetFileNameWithoutExtension('$(_AndroidHotReloadAgentAssemblyPath)'))</_AndroidHotReloadAgentAssemblyName>
+    </PropertyGroup>
+
+    <!--
+      Update DOTNET_STARTUP_HOOKS in @(RuntimeEnvironmentVariable) to use just the assembly name.
+      The full path doesn't work on Android since the DLL is deployed alongside the app.
+    -->
+    <ItemGroup Condition=" '$(_AndroidHotReloadAgentAssemblyName)' != '' ">
+      <RuntimeEnvironmentVariable Remove="DOTNET_STARTUP_HOOKS" />
+      <RuntimeEnvironmentVariable Include="DOTNET_STARTUP_HOOKS" Value="$(_AndroidHotReloadAgentAssemblyName)" />
+      <!-- Set STARTUP_HOOKS via RuntimeHostConfigurationOption for MonoVM (read by Mono runtime) -->
+      <RuntimeHostConfigurationOption Include="STARTUP_HOOKS" Value="$(_AndroidHotReloadAgentAssemblyName)" Condition=" '$(UseMonoRuntime)' == 'true' " />
+    </ItemGroup>
+
+  </Target>
+
+  <!--
+    _AndroidConfigureAdbReverse:
+    Sets up adb reverse port forwarding when using WebSocket endpoint from @(RuntimeEnvironmentVariable).
+    Extracts the port from DOTNET_WATCH_HOTRELOAD_WEBSOCKET_ENDPOINT and sets up reverse forwarding.
+    This allows the device/emulator to connect back to the host machine.
+  -->
+  <Target Name="_AndroidConfigureAdbReverse"
+          Condition=" '@(RuntimeEnvironmentVariable)' != '' "
+          DependsOnTargets="_AndroidAdbToolPath">
+
+    <!-- Extract the WebSocket endpoint URL and parse the port -->
+    <PropertyGroup>
+      <_AndroidWebSocketEndpoint>@(RuntimeEnvironmentVariable->WithMetadataValue('Identity', 'DOTNET_WATCH_HOTRELOAD_WEBSOCKET_ENDPOINT')->'%(Value)')</_AndroidWebSocketEndpoint>
+    </PropertyGroup>
+
+    <!-- Parse port from WebSocket URL (e.g., ws://localhost:9000 or http://localhost:9000) -->
+    <PropertyGroup Condition=" '$(_AndroidWebSocketEndpoint)' != '' ">
+      <_AndroidWebSocketPort>$([System.UriBuilder]::new('$(_AndroidWebSocketEndpoint)').Port)</_AndroidWebSocketPort>
+      <!-- UriBuilder.Port returns -1 when no port is specified -->
+      <_AndroidWebSocketPort Condition=" '$(_AndroidWebSocketPort)' == '-1' "></_AndroidWebSocketPort>
+    </PropertyGroup>
+
+    <Exec Condition=" '$(_AndroidWebSocketPort)' != '' "
+          Command="&quot;$(_AdbToolPath)&quot; reverse tcp:$(_AndroidWebSocketPort) tcp:$(_AndroidWebSocketPort)" />
+
+  </Target>
+
+</Project>
+
diff --git a/src/Xamarin.Android.Build.Tasks/Microsoft.Android.Sdk/targets/Microsoft.Android.Sdk.ProjectCapabilities.targets b/src/Xamarin.Android.Build.Tasks/Microsoft.Android.Sdk/targets/Microsoft.Android.Sdk.ProjectCapabilities.targets
index a8b04059e23..454e67cd0bf 100644
--- a/src/Xamarin.Android.Build.Tasks/Microsoft.Android.Sdk/targets/Microsoft.Android.Sdk.ProjectCapabilities.targets
+++ b/src/Xamarin.Android.Build.Tasks/Microsoft.Android.Sdk/targets/Microsoft.Android.Sdk.ProjectCapabilities.targets
@@ -17,6 +17,7 @@ Docs about @(ProjectCapability):
     <ProjectCapability Include="Mobile" />
     <ProjectCapability Include="Android" />
     <ProjectCapability Include="AndroidApplication" Condition="$(AndroidApplication)" />
+    <ProjectCapability Include="HotReloadWebSockets" Condition="$(AndroidApplication)" />
     <ProjectCapability Condition="'$(_KeepLaunchProfiles)' != 'true'" Remove="LaunchProfiles" />
   </ItemGroup>
 
diff --git a/src/Xamarin.Android.Build.Tasks/Xamarin.Android.Common.targets b/src/Xamarin.Android.Build.Tasks/Xamarin.Android.Common.targets
index ee75d41fb97..b49c0d25b9f 100644
--- a/src/Xamarin.Android.Build.Tasks/Xamarin.Android.Common.targets
+++ b/src/Xamarin.Android.Build.Tasks/Xamarin.Android.Common.targets
@@ -1773,7 +1773,7 @@ because xbuild doesn't support framework reference assemblies.
   </PrepareAbiItems>
 </Target>
 
-<Target Name="_GenerateEnvironmentFiles">
+<Target Name="_GenerateEnvironmentFiles" DependsOnTargets="_AndroidConfigureHotReloadEnvironment">
   <ItemGroup>
     <_GeneratedAndroidEnvironment Include="mono.enable_assembly_preload=0" Condition=" '$(AndroidEnablePreloadAssemblies)' != 'True' " />
     <_GeneratedAndroidEnvironment Include="DOTNET_MODIFIABLE_ASSEMBLIES=Debug" Condition=" '$(AndroidIncludeDebugSymbols)' == 'true' and '$(AndroidUseInterpreter)' == 'true' " />