diff --git a/src/NodePilot.Api/Configuration/RuntimeOverridesWriter.cs b/src/NodePilot.Api/Configuration/RuntimeOverridesWriter.cs
index 7d71296e..d27ac28b 100644
--- a/src/NodePilot.Api/Configuration/RuntimeOverridesWriter.cs
+++ b/src/NodePilot.Api/Configuration/RuntimeOverridesWriter.cs
@@ -2,6 +2,7 @@
 using System.Text;
 using System.Text.Json;
 using System.Text.Json.Nodes;
+using Microsoft.Extensions.Configuration.Json;
 using NodePilot.Core.Interfaces;
 
 namespace NodePilot.Api.Configuration;
@@ -127,11 +128,11 @@ private static bool ReencryptValues(JsonNode node, ISecretProtector protector, C
 
     internal static void ReplaceWithoutBackup(string path, JsonObject root)
     {
+        var content = SerializeAndValidate(root);
         var temporary = path + ".migration." + Guid.NewGuid().ToString("N") + ".tmp";
         try
         {
-            File.WriteAllText(temporary, root.ToJsonString(new JsonSerializerOptions { WriteIndented = true }),
-                new UTF8Encoding(encoderShouldEmitUTF8Identifier: false));
+            File.WriteAllBytes(temporary, content);
             try { File.Replace(temporary, path, destinationBackupFileName: null); }
             catch (Exception ex) when (ex is IOException or PlatformNotSupportedException or UnauthorizedAccessException)
             {
@@ -147,13 +148,40 @@ internal static void ReplaceWithoutBackup(string path, JsonObject root)
     /// </summary>
     public JsonObject ReadOrEmpty()
     {
-        if (!File.Exists(_path)) return new JsonObject();
+        var nodeOptions = new JsonNodeOptions { PropertyNameCaseInsensitive = true };
+        if (!File.Exists(_path)) return new JsonObject(nodeOptions);
         var raw = File.ReadAllText(_path);
-        if (string.IsNullOrWhiteSpace(raw)) return new JsonObject();
-        var parsed = JsonNode.Parse(raw) as JsonObject
+        if (string.IsNullOrWhiteSpace(raw)) return new JsonObject(nodeOptions);
+        var parsed = JsonNode.Parse(raw, documentOptions:
+            new JsonDocumentOptions { CommentHandling = JsonCommentHandling.Skip, AllowTrailingCommas = true }) as JsonObject
             ?? throw new InvalidOperationException(
                 $"Runtime overrides file '{_path}' must contain a JSON object at the root.");
-        return parsed;
+        return NormalizeConfigurationKeys(parsed).AsObject();
+    }
+
+    private static JsonNode NormalizeConfigurationKeys(JsonNode node)
+    {
+        if (node is JsonObject source)
+        {
+            var result = new JsonObject(new JsonNodeOptions { PropertyNameCaseInsensitive = true });
+            MergeConfigurationObject(result, source);
+            return result;
+        }
+        if (node is JsonArray array)
+            return new JsonArray(array.Select(child => child is null ? null : NormalizeConfigurationKeys(child)).ToArray());
+        return node.DeepClone();
+    }
+
+    private static void MergeConfigurationObject(JsonObject target, JsonObject source)
+    {
+        foreach (var (key, value) in source)
+        {
+            // IConfiguration permits case-variant sections when their leaf keys are disjoint.
+            if (target[key] is JsonObject existing && value is JsonObject nested)
+                MergeConfigurationObject(existing, nested);
+            else
+                target.Add(key, value is null ? null : NormalizeConfigurationKeys(value));
+        }
     }
 
     /// <summary>
@@ -463,9 +491,9 @@ private void EnsureDirectoryExists()
 
     private void WriteAtomic(JsonObject root)
     {
+        var content = SerializeAndValidate(root);
         var tmp = _path + ".tmp";
-        var json = root.ToJsonString(new JsonSerializerOptions { WriteIndented = true });
-        File.WriteAllText(tmp, json, new UTF8Encoding(encoderShouldEmitUTF8Identifier: false));
+        File.WriteAllBytes(tmp, content);
 
         if (!File.Exists(_path))
         {
@@ -497,6 +525,16 @@ private void WriteAtomic(JsonObject root)
         RotateBackups();
     }
 
+    private static byte[] SerializeAndValidate(JsonObject root)
+    {
+        var content = Encoding.UTF8.GetBytes(root.ToJsonString(new JsonSerializerOptions { WriteIndented = true }));
+        // The encrypting production provider uses this parser before decrypting leaf values.
+        using var provider = new JsonConfigurationProvider(new JsonConfigurationSource());
+        using var stream = new MemoryStream(content, writable: false);
+        provider.Load(stream);
+        return content;
+    }
+
     private void RotateBackups()
     {
         var dir = Path.GetDirectoryName(_path);
diff --git a/tests/NodePilot.Api.Tests/Configuration/RuntimeOverridesWriterTests.cs b/tests/NodePilot.Api.Tests/Configuration/RuntimeOverridesWriterTests.cs
index cec48ede..164dbc3a 100644
--- a/tests/NodePilot.Api.Tests/Configuration/RuntimeOverridesWriterTests.cs
+++ b/tests/NodePilot.Api.Tests/Configuration/RuntimeOverridesWriterTests.cs
@@ -1,4 +1,5 @@
 using System.Text.Json.Nodes;
+using Microsoft.Extensions.Configuration;
 using FluentAssertions;
 using Microsoft.Extensions.Logging.Abstractions;
 using NodePilot.Api.Configuration;
@@ -33,6 +34,88 @@ private RuntimeOverridesWriter NewWriter(string? subPath = null)
         return new RuntimeOverridesWriter(path, NullLogger<RuntimeOverridesWriter>.Instance);
     }
 
+    [Fact]
+    public void TryUpdateSectionAtomic_LowerCaseSection_RemainsLoadable()
+    {
+        var writer = NewWriter();
+        File.WriteAllText(writer.OverridesPath, """{"stats":{"RefreshIntervalMinutes":5,"WindowDays":7}}""");
+        var result = writer.TryUpdateSectionAtomic("Stats", writer.ComputeSectionEtag("Stats"),
+            new JsonObject { ["RefreshIntervalMinutes"] = 10, ["WindowDays"] = 7 },
+            null, "admin", DateTimeOffset.UtcNow);
+
+        result.Success.Should().BeTrue();
+        var config = new ConfigurationBuilder().AddJsonFile(writer.OverridesPath).Build();
+        using var disposable = (IDisposable)config;
+        config["Stats:RefreshIntervalMinutes"].Should().Be("10");
+        config["Stats:WindowDays"].Should().Be("7");
+        writer.ReadOrEmpty().Count(pair => pair.Key.Equals("Stats", StringComparison.OrdinalIgnoreCase)).Should().Be(1);
+    }
+
+    [Fact]
+    public void TryUpdateSectionAtomic_MixedCaseNestedPath_PreservesSiblingAndReadsExistingValue()
+    {
+        var writer = NewWriter();
+        File.WriteAllText(writer.OverridesPath,
+            """{"retention":{"executions":{"MaxAgeDays":7},"auditlog":{"MaxAgeDays":90}}}""");
+        (writer.ReadSection("Retention:Executions")?["MaxAgeDays"]?.GetValue<int>()).Should().Be(7);
+
+        var result = writer.TryUpdateSectionAtomic("Retention:Executions", writer.ComputeSectionEtag("Retention:Executions"),
+            new JsonObject { ["MaxAgeDays"] = 14 }, null, "admin", DateTimeOffset.UtcNow);
+
+        result.Success.Should().BeTrue();
+        var config = new ConfigurationBuilder().AddJsonFile(writer.OverridesPath).Build();
+        using var disposable = (IDisposable)config;
+        config["Retention:Executions:MaxAgeDays"].Should().Be("14");
+        config["Retention:AuditLog:MaxAgeDays"].Should().Be("90");
+    }
+
+    [Theory]
+    [InlineData(false)]
+    [InlineData(true)]
+    public void Write_DuplicateFlattenedKeys_RejectsCandidateAndPreservesOriginal(bool replace)
+    {
+        var writer = NewWriter();
+        const string original = """{"Stats":{"WindowDays":7}}""";
+        File.WriteAllText(writer.OverridesPath, original);
+        var invalid = new JsonObject
+        {
+            ["Stats"] = new JsonObject { ["WindowDays"] = 14 },
+            ["stats:windowdays"] = 30
+        };
+
+        var act = () =>
+        {
+            if (replace) writer.ReplaceAll(invalid);
+            else writer.MutateAndWrite(root => root["stats:windowdays"] = 30);
+        };
+
+        act.Should().Throw<FormatException>();
+        File.ReadAllText(writer.OverridesPath).Should().Be(original);
+        Directory.GetFiles(_tempDir, "*.bak.*").Should().BeEmpty();
+        Directory.GetFiles(_tempDir, "*.tmp").Should().BeEmpty();
+    }
+
+    [Fact]
+    public void TryUpdateSectionAtomic_DisjointCaseVariantSections_MergesTheirExistingValues()
+    {
+        var writer = NewWriter();
+        File.WriteAllText(writer.OverridesPath,
+            """{"retention":{"executions":{"MaxAgeDays":7}},"Retention":{"auditlog":{"MaxAgeDays":90}}}""");
+        var before = new ConfigurationBuilder().AddJsonFile(writer.OverridesPath).Build();
+        using var beforeDisposable = (IDisposable)before;
+        before["Retention:Executions:MaxAgeDays"].Should().Be("7");
+        before["Retention:AuditLog:MaxAgeDays"].Should().Be("90");
+
+        var result = writer.TryUpdateSectionAtomic("Retention:Executions", writer.ComputeSectionEtag("Retention:Executions"),
+            new JsonObject { ["MaxAgeDays"] = 14 }, null, "admin", DateTimeOffset.UtcNow);
+
+        result.Success.Should().BeTrue();
+        var after = new ConfigurationBuilder().AddJsonFile(writer.OverridesPath).Build();
+        using var afterDisposable = (IDisposable)after;
+        after["Retention:Executions:MaxAgeDays"].Should().Be("14");
+        after["Retention:AuditLog:MaxAgeDays"].Should().Be("90");
+    }
+
     [Fact]
     public void ReadOrEmpty_FileMissing_ReturnsEmptyObject()
     {