diff --git a/src/mono/nuget/Microsoft.NET.Sdk.WebAssembly.Pack/build/Microsoft.NET.Sdk.WebAssembly.Browser.targets b/src/mono/nuget/Microsoft.NET.Sdk.WebAssembly.Pack/build/Microsoft.NET.Sdk.WebAssembly.Browser.targets
index 48360c01d7e993..3b5d827b381355 100644
--- a/src/mono/nuget/Microsoft.NET.Sdk.WebAssembly.Pack/build/Microsoft.NET.Sdk.WebAssembly.Browser.targets
+++ b/src/mono/nuget/Microsoft.NET.Sdk.WebAssembly.Pack/build/Microsoft.NET.Sdk.WebAssembly.Browser.targets
@@ -703,7 +703,7 @@ Copyright (c) .NET Foundation. All rights reserved.
   <Target Name="_WriteBuildWasmBootJsonFile"
     DependsOnTargets="_WriteWasmBootJsonBuildPropertyStamp"
     Condition="'$(WasmBuildingForNestedPublish)' != 'true'"
-    Inputs="@(IntermediateAssembly);@(WasmStaticWebAsset);@(_WasmJsModuleCandidatesForBuild);@(_WasmFilesToIncludeInFileSystemStaticWebAsset);@(_WasmJsConfigStaticWebAsset);@(_WasmDotnetJsForBuild);@(WasmBootConfigExtension);$(ProjectRuntimeConfigFilePath);$(MSBuildProjectFullPath);$(MSBuildThisFileFullPath);$(_WebAssemblySdkTasksAssembly);$(IntermediateOutputPath)wasm-bootjson-build.stamp"
+    Inputs="@(IntermediateAssembly);@(WasmStaticWebAsset);@(_WasmJsModuleCandidatesForBuild);@(_WasmFilesToIncludeInFileSystemStaticWebAsset);@(_WasmJsConfigStaticWebAsset);@(_WasmDotnetJsForBuild);@(WasmBootConfigExtension);$(ProjectRuntimeConfigFilePath);$(ProjectRuntimeConfigDevFilePath);$(MSBuildProjectFullPath);$(MSBuildThisFileFullPath);$(_WebAssemblySdkTasksAssembly);$(IntermediateOutputPath)wasm-bootjson-build.stamp"
     Outputs="$(IntermediateOutputPath)wasm-bootjson-build.complete.stamp">
 
     <GenerateWasmBootJson
@@ -727,6 +727,7 @@ Copyright (c) .NET Foundation. All rights reserved.
       EnvVariables="@(WasmEnvironmentVariable)"
       Profilers="$(WasmProfilers)"
       RuntimeConfigJsonPath="$(ProjectRuntimeConfigFilePath)"
+      RuntimeConfigDevJsonPath="$(ProjectRuntimeConfigDevFilePath)"
       TargetFrameworkVersion="$(TargetFrameworkVersion)"
       ModuleAfterConfigLoaded="@(WasmModuleAfterConfigLoaded)"
       ModuleAfterRuntimeReady="@(WasmModuleAfterRuntimeReady)"
diff --git a/src/tasks.tests/Microsoft.NET.Sdk.WebAssembly.Pack.Tasks.Tests/GenerateWasmBootJsonTests.cs b/src/tasks.tests/Microsoft.NET.Sdk.WebAssembly.Pack.Tasks.Tests/GenerateWasmBootJsonTests.cs
new file mode 100644
index 00000000000000..5c52092227b342
--- /dev/null
+++ b/src/tasks.tests/Microsoft.NET.Sdk.WebAssembly.Pack.Tasks.Tests/GenerateWasmBootJsonTests.cs
@@ -0,0 +1,183 @@
+// Licensed to the .NET Foundation under one or more agreements.
+// The .NET Foundation licenses this file to you under the MIT license.
+
+using System.Collections.Generic;
+using System.IO;
+using System.Text.Json;
+using Xunit;
+
+namespace Microsoft.NET.Sdk.WebAssembly.Tests;
+
+public class GenerateWasmBootJsonTests
+{
+    [Fact]
+    public void ReadRuntimeConfigFiles_NullMainConfigPath_ReturnsNull()
+    {
+        var result = GenerateWasmBootJson.ReadRuntimeConfigFiles(null, null);
+
+        Assert.Null(result);
+    }
+
+    [Fact]
+    public void ReadRuntimeConfigFiles_MainConfigNotExists_ReturnsNull()
+    {
+        using var dir = new TempDirectory();
+        var nonExistentPath = Path.Combine(dir.Path, "does-not-exist.runtimeconfig.json");
+        var result = GenerateWasmBootJson.ReadRuntimeConfigFiles(nonExistentPath, null);
+
+        Assert.Null(result);
+    }
+
+    [Fact]
+    public void ReadRuntimeConfigFiles_DevConfigPreservesBooleanAndNumericTypes()
+    {
+        using var dir = new TempDirectory();
+        var mainConfig = WriteRuntimeConfig(dir.Path, "App.runtimeconfig.json",
+            configProperties: new() { ["key1"] = "value1" });
+        // Write dev config with native JSON boolean and number (not string) values.
+        var devConfigPath = Path.Combine(dir.Path, "App.runtimeconfig.dev.json");
+        File.WriteAllText(devConfigPath, """
+            {
+              "runtimeOptions": {
+                "configProperties": {
+                  "System.HotReload.Enable": true,
+                  "System.HotReload.MaxRetries": 10
+                }
+              }
+            }
+            """);
+
+        var result = GenerateWasmBootJson.ReadRuntimeConfigFiles(mainConfig, devConfigPath);
+
+        Assert.NotNull(result?.runtimeOptions?.configProperties);
+        var props = result!.runtimeOptions!.configProperties!;
+        Assert.Equal(JsonValueKind.True, ((JsonElement)props["System.HotReload.Enable"]).ValueKind);
+        Assert.Equal(JsonValueKind.Number, ((JsonElement)props["System.HotReload.MaxRetries"]).ValueKind);
+        Assert.Equal(10, ((JsonElement)props["System.HotReload.MaxRetries"]).GetInt32());
+    }
+
+    [Fact]
+    public void ReadRuntimeConfigFiles_MainConfigOnly_ReturnsMainProperties()
+    {
+        using var dir = new TempDirectory();
+        var mainConfig = WriteRuntimeConfig(dir.Path, "App.runtimeconfig.json",
+            configProperties: new() { ["key1"] = "value1", ["key2"] = "42" });
+
+        var result = GenerateWasmBootJson.ReadRuntimeConfigFiles(mainConfig, null);
+
+        Assert.NotNull(result);
+        Assert.NotNull(result.runtimeOptions?.configProperties);
+        Assert.Equal("value1", result.runtimeOptions!.configProperties!["key1"].ToString());
+        Assert.Equal("42", result.runtimeOptions.configProperties["key2"].ToString());
+    }
+
+    [Fact]
+    public void ReadRuntimeConfigFiles_DevConfigNotExists_ReturnsMainPropertiesUnchanged()
+    {
+        using var dir = new TempDirectory();
+        var mainConfig = WriteRuntimeConfig(dir.Path, "App.runtimeconfig.json",
+            configProperties: new() { ["key1"] = "value1" });
+        var devConfigPath = Path.Combine(dir.Path, "App.runtimeconfig.dev.json");
+
+        var result = GenerateWasmBootJson.ReadRuntimeConfigFiles(mainConfig, devConfigPath);
+
+        Assert.NotNull(result);
+        Assert.Equal("value1", result.runtimeOptions?.configProperties?["key1"].ToString());
+    }
+
+    [Fact]
+    public void ReadRuntimeConfigFiles_DevConfigAddsNewProperty()
+    {
+        using var dir = new TempDirectory();
+        var mainConfig = WriteRuntimeConfig(dir.Path, "App.runtimeconfig.json",
+            configProperties: new() { ["key1"] = "value1" });
+        var devConfig = WriteRuntimeConfig(dir.Path, "App.runtimeconfig.dev.json",
+            configProperties: new() { ["key2"] = "value2" });
+
+        var result = GenerateWasmBootJson.ReadRuntimeConfigFiles(mainConfig, devConfig);
+
+        Assert.NotNull(result?.runtimeOptions?.configProperties);
+        Assert.Equal("value1", result!.runtimeOptions!.configProperties!["key1"].ToString());
+        Assert.Equal("value2", result.runtimeOptions.configProperties["key2"].ToString());
+    }
+
+    [Fact]
+    public void ReadRuntimeConfigFiles_DevConfigOverridesMainProperty()
+    {
+        using var dir = new TempDirectory();
+        var mainConfig = WriteRuntimeConfig(dir.Path, "App.runtimeconfig.json",
+            configProperties: new() { ["System.Runtime.Feature"] = "false" });
+        var devConfig = WriteRuntimeConfig(dir.Path, "App.runtimeconfig.dev.json",
+            configProperties: new() { ["System.Runtime.Feature"] = "true" });
+
+        var result = GenerateWasmBootJson.ReadRuntimeConfigFiles(mainConfig, devConfig);
+
+        Assert.NotNull(result?.runtimeOptions?.configProperties);
+        Assert.Equal("true", result!.runtimeOptions!.configProperties!["System.Runtime.Feature"].ToString());
+    }
+
+    [Fact]
+    public void ReadRuntimeConfigFiles_DevConfigMergesWhenMainHasNoConfigProperties()
+    {
+        using var dir = new TempDirectory();
+        var mainConfig = WriteRuntimeConfig(dir.Path, "App.runtimeconfig.json",
+            configProperties: null);
+        var devConfig = WriteRuntimeConfig(dir.Path, "App.runtimeconfig.dev.json",
+            configProperties: new() { ["System.HotReload.Enable"] = "true" });
+
+        var result = GenerateWasmBootJson.ReadRuntimeConfigFiles(mainConfig, devConfig);
+
+        Assert.NotNull(result?.runtimeOptions?.configProperties);
+        Assert.Equal("true", result!.runtimeOptions!.configProperties!["System.HotReload.Enable"].ToString());
+    }
+
+    [Fact]
+    public void ReadRuntimeConfigFiles_DevConfigEmptyProperties_DoesNotAlterResult()
+    {
+        using var dir = new TempDirectory();
+        var mainConfig = WriteRuntimeConfig(dir.Path, "App.runtimeconfig.json",
+            configProperties: new() { ["key1"] = "value1" });
+        var devConfig = WriteRuntimeConfig(dir.Path, "App.runtimeconfig.dev.json",
+            configProperties: new());
+
+        var result = GenerateWasmBootJson.ReadRuntimeConfigFiles(mainConfig, devConfig);
+
+        Assert.NotNull(result?.runtimeOptions?.configProperties);
+        Assert.Single(result!.runtimeOptions!.configProperties!);
+        Assert.Equal("value1", result.runtimeOptions.configProperties["key1"].ToString());
+    }
+
+    private static string WriteRuntimeConfig(string dir, string fileName, Dictionary<string, string>? configProperties)
+    {
+        var path = Path.Combine(dir, fileName);
+        using var stream = File.OpenWrite(path);
+        using var writer = new Utf8JsonWriter(stream, new JsonWriterOptions { Indented = true });
+        writer.WriteStartObject();
+        writer.WritePropertyName("runtimeOptions");
+        writer.WriteStartObject();
+        if (configProperties is not null)
+        {
+            writer.WritePropertyName("configProperties");
+            writer.WriteStartObject();
+            foreach (var (key, value) in configProperties)
+                writer.WriteString(key, value);
+            writer.WriteEndObject();
+        }
+        writer.WriteEndObject();
+        writer.WriteEndObject();
+        return path;
+    }
+
+    private sealed class TempDirectory : System.IDisposable
+    {
+        public string Path { get; } = System.IO.Path.Combine(System.IO.Path.GetTempPath(), System.IO.Path.GetRandomFileName());
+
+        public TempDirectory() => Directory.CreateDirectory(Path);
+
+        public void Dispose()
+        {
+            // Silently ignore cleanup failures to avoid masking actual test failures.
+            try { Directory.Delete(Path, recursive: true); } catch { }
+        }
+    }
+}
diff --git a/src/tasks.tests/Microsoft.NET.Sdk.WebAssembly.Pack.Tasks.Tests/Microsoft.NET.Sdk.WebAssembly.Pack.Tasks.Tests.csproj b/src/tasks.tests/Microsoft.NET.Sdk.WebAssembly.Pack.Tasks.Tests/Microsoft.NET.Sdk.WebAssembly.Pack.Tasks.Tests.csproj
new file mode 100644
index 00000000000000..9adcea8712095e
--- /dev/null
+++ b/src/tasks.tests/Microsoft.NET.Sdk.WebAssembly.Pack.Tasks.Tests/Microsoft.NET.Sdk.WebAssembly.Pack.Tasks.Tests.csproj
@@ -0,0 +1,14 @@
+<Project Sdk="Microsoft.NET.Sdk">
+
+  <PropertyGroup>
+    <TargetFramework>$(NetCoreAppToolCurrent)</TargetFramework>
+    <Nullable>enable</Nullable>
+  </PropertyGroup>
+
+  <ItemGroup>
+    <PackageReference Include="Microsoft.Build.Framework" Version="$(MicrosoftBuildFrameworkVersion)" />
+    <PackageReference Include="Microsoft.Build.Utilities.Core" Version="$(MicrosoftBuildUtilitiesCoreVersion)" />
+    <ProjectReference Include="..\..\tasks\Microsoft.NET.Sdk.WebAssembly.Pack.Tasks\Microsoft.NET.Sdk.WebAssembly.Pack.Tasks.csproj" />
+  </ItemGroup>
+
+</Project>
diff --git a/src/tasks/Microsoft.NET.Sdk.WebAssembly.Pack.Tasks/GenerateWasmBootJson.cs b/src/tasks/Microsoft.NET.Sdk.WebAssembly.Pack.Tasks/GenerateWasmBootJson.cs
index 07f5daa0ea14ab..784b2a77d71755 100644
--- a/src/tasks/Microsoft.NET.Sdk.WebAssembly.Pack.Tasks/GenerateWasmBootJson.cs
+++ b/src/tasks/Microsoft.NET.Sdk.WebAssembly.Pack.Tasks/GenerateWasmBootJson.cs
@@ -61,6 +61,8 @@ public class GenerateWasmBootJson : Task
 
     public string? RuntimeConfigJsonPath { get; set; }
 
+    public string? RuntimeConfigDevJsonPath { get; set; }
+
     public string Jiterpreter { get; set; }
 
     public string RuntimeOptions { get; set; }
@@ -463,12 +465,7 @@ private void WriteBootConfig(string entryAssemblyName)
             }
         }
 
-        if (RuntimeConfigJsonPath != null && File.Exists(RuntimeConfigJsonPath))
-        {
-            using var fs = File.OpenRead(RuntimeConfigJsonPath);
-            var runtimeConfig = JsonSerializer.Deserialize<RuntimeConfigData>(fs, BootJsonBuilderHelper.JsonOptions);
-            result.runtimeConfig = runtimeConfig;
-        }
+        result.runtimeConfig = ReadRuntimeConfigFiles(RuntimeConfigJsonPath, IsPublish ? null : RuntimeConfigDevJsonPath);
 
         Profilers ??= Array.Empty<string>();
         var browserProfiler = Profilers.FirstOrDefault(p => p.StartsWith("browser:"));
@@ -569,4 +566,36 @@ private Version ParsedTargetFrameworkVersion
     private bool IsTargeting90OrLater() => ParsedTargetFrameworkVersion >= version90;
     private bool IsTargeting100OrLater() => ParsedTargetFrameworkVersion >= version100;
     private bool IsTargeting110OrLater() => ParsedTargetFrameworkVersion >= version110;
+
+    /// <summary>
+    /// Reads the main runtimeconfig.json and merges <c>configProperties</c> from the companion
+    /// runtimeconfig.dev.json (when it exists) into the result. Dev config values take precedence.
+    /// </summary>
+    internal static RuntimeConfigData? ReadRuntimeConfigFiles(string? mainConfigPath, string? devConfigPath)
+    {
+        if (!File.Exists(mainConfigPath))
+            return null;
+
+        using var fs = File.OpenRead(mainConfigPath);
+        var runtimeConfig = JsonSerializer.Deserialize<RuntimeConfigData>(fs, BootJsonBuilderHelper.JsonOptions);
+
+        if (File.Exists(devConfigPath))
+        {
+            // Merge overrides from runtimeconfig.dev.json (e.g. Hot Reload switches set by the SDK in debug builds).
+            using var devFs = File.OpenRead(devConfigPath);
+            var devRuntimeConfig = JsonSerializer.Deserialize<RuntimeConfigData>(devFs, BootJsonBuilderHelper.JsonOptions);
+            if (devRuntimeConfig?.runtimeOptions?.configProperties is { } devProps && devProps.Count > 0)
+            {
+                runtimeConfig ??= new RuntimeConfigData();
+                runtimeConfig.runtimeOptions ??= new RuntimeOptionsData();
+                runtimeConfig.runtimeOptions.configProperties ??= new Dictionary<string, object>();
+                foreach (var kvp in devProps)
+                {
+                    runtimeConfig.runtimeOptions.configProperties[kvp.Key] = kvp.Value;
+                }
+            }
+        }
+
+        return runtimeConfig;
+    }
 }
diff --git a/src/tasks/Microsoft.NET.Sdk.WebAssembly.Pack.Tasks/Microsoft.NET.Sdk.WebAssembly.Pack.Tasks.csproj b/src/tasks/Microsoft.NET.Sdk.WebAssembly.Pack.Tasks/Microsoft.NET.Sdk.WebAssembly.Pack.Tasks.csproj
index 90267a01c8e52a..ecf3510c8914df 100644
--- a/src/tasks/Microsoft.NET.Sdk.WebAssembly.Pack.Tasks/Microsoft.NET.Sdk.WebAssembly.Pack.Tasks.csproj
+++ b/src/tasks/Microsoft.NET.Sdk.WebAssembly.Pack.Tasks/Microsoft.NET.Sdk.WebAssembly.Pack.Tasks.csproj
@@ -17,6 +17,7 @@
   </PropertyGroup>
 
   <ItemGroup>
+    <InternalsVisibleTo Include="Microsoft.NET.Sdk.WebAssembly.Pack.Tasks.Tests" />
     <Compile Include="..\Common\Utils.cs" />
     <Compile Include="..\WasmAppBuilder\WebcilConverter.cs" />
     <Compile Include="..\WasmAppBuilder\LogAdapter.cs" />