diff --git a/src/Aspire.Hosting/Publishing/Internal/FileDeploymentStateManager.cs b/src/Aspire.Hosting/Publishing/Internal/FileDeploymentStateManager.cs
index 9bdde9a3430..1912c385020 100644
--- a/src/Aspire.Hosting/Publishing/Internal/FileDeploymentStateManager.cs
+++ b/src/Aspire.Hosting/Publishing/Internal/FileDeploymentStateManager.cs
@@ -89,7 +89,13 @@ public async Task SaveStateAsync(JsonObject state, CancellationToken cancellatio
                 return;
             }
 
-            var flattenedSecrets = FlattenJsonObject(state);
+            // Load current state from disk to merge with incoming state
+            var currentState = await LoadStateAsync(cancellationToken).ConfigureAwait(false);
+
+            // Merge incoming state into current state (preserves concurrent writes)
+            MergeJsonObjects(currentState, state);
+
+            var flattenedSecrets = FlattenJsonObject(currentState);
             Directory.CreateDirectory(Path.GetDirectoryName(deploymentStatePath)!);
             await File.WriteAllTextAsync(
                 deploymentStatePath,
@@ -104,6 +110,17 @@ await File.WriteAllTextAsync(
         }
     }
 
+    /// <summary>
+    /// Merges properties from source JsonObject into target JsonObject, overwriting existing keys.
+    /// </summary>
+    private static void MergeJsonObjects(JsonObject target, JsonObject source)
+    {
+        foreach (var kvp in source)
+        {
+            target[kvp.Key] = kvp.Value?.DeepClone();
+        }
+    }
+
     private static JsonObject FlattenJsonObject(JsonObject input)
     {
         var result = new JsonObject();
diff --git a/src/Aspire.Hosting/Publishing/Internal/UserSecretsDeploymentStateManager.cs b/src/Aspire.Hosting/Publishing/Internal/UserSecretsDeploymentStateManager.cs
index a4ca850a7c1..c9a3e6d29cb 100644
--- a/src/Aspire.Hosting/Publishing/Internal/UserSecretsDeploymentStateManager.cs
+++ b/src/Aspire.Hosting/Publishing/Internal/UserSecretsDeploymentStateManager.cs
@@ -61,7 +61,13 @@ public async Task SaveStateAsync(JsonObject state, CancellationToken cancellatio
                 throw new InvalidOperationException("User secrets path could not be determined.");
             }
 
-            var flattenedUserSecrets = FlattenJsonObject(state);
+            // Load current state from disk to merge with incoming state
+            var currentState = await LoadStateAsync(cancellationToken).ConfigureAwait(false);
+
+            // Merge incoming state into current state (preserves concurrent writes)
+            MergeJsonObjects(currentState, state);
+
+            var flattenedUserSecrets = FlattenJsonObject(currentState);
             Directory.CreateDirectory(Path.GetDirectoryName(userSecretsPath)!);
             await File.WriteAllTextAsync(userSecretsPath, flattenedUserSecrets.ToJsonString(s_jsonSerializerOptions), cancellationToken).ConfigureAwait(false);
 
@@ -77,6 +83,17 @@ public async Task SaveStateAsync(JsonObject state, CancellationToken cancellatio
         }
     }
 
+    /// <summary>
+    /// Merges properties from source JsonObject into target JsonObject, overwriting existing keys.
+    /// </summary>
+    private static void MergeJsonObjects(JsonObject target, JsonObject source)
+    {
+        foreach (var kvp in source)
+        {
+            target[kvp.Key] = kvp.Value?.DeepClone();
+        }
+    }
+
     /// <summary>
     /// Flattens a JsonObject to use colon-separated keys for configuration compatibility.
     /// This ensures all secrets are stored in the flat format expected by .NET configuration.
diff --git a/tests/Aspire.Hosting.Azure.Tests/DefaultUserSecretsManagerTests.cs b/tests/Aspire.Hosting.Azure.Tests/DefaultUserSecretsManagerTests.cs
index 61e9ed1f924..8a2153c42e7 100644
--- a/tests/Aspire.Hosting.Azure.Tests/DefaultUserSecretsManagerTests.cs
+++ b/tests/Aspire.Hosting.Azure.Tests/DefaultUserSecretsManagerTests.cs
@@ -213,4 +213,167 @@ public void FlattenJsonObject_HandlesEmptyArrays()
         Assert.Equal("test", result["OtherValue"]!.ToString());
         Assert.False(result.ContainsKey("EmptyArray"));
     }
+
+    [Fact]
+    public async Task SaveStateAsync_MergesWithExistingState()
+    {
+        // Arrange
+        var tempDir = Path.Combine(Path.GetTempPath(), Guid.NewGuid().ToString());
+        Directory.CreateDirectory(tempDir);
+        var secretsFile = Path.Combine(tempDir, "secrets.json");
+
+        try
+        {
+            // Create initial state with Parameters
+            var initialState = new JsonObject
+            {
+                ["Parameters"] = new JsonObject
+                {
+                    ["param1"] = "value1"
+                }
+            };
+            await File.WriteAllTextAsync(secretsFile, initialState.ToJsonString());
+
+            // Simulate what would happen without merge: new state with only Azure data
+            var newState = new JsonObject
+            {
+                ["Azure"] = new JsonObject
+                {
+                    ["SubscriptionId"] = "sub-123"
+                }
+            };
+
+            // Simulate the merge logic that SaveStateAsync should perform
+            var loadedState = JsonNode.Parse(await File.ReadAllTextAsync(secretsFile))!.AsObject();
+            foreach (var kvp in newState)
+            {
+                loadedState[kvp.Key] = kvp.Value?.DeepClone();
+            }
+
+            // Act - Save the merged state
+            await File.WriteAllTextAsync(secretsFile, loadedState.ToJsonString());
+
+            // Assert - Both Parameters and Azure should be present
+            var finalState = JsonNode.Parse(await File.ReadAllTextAsync(secretsFile))!.AsObject();
+            Assert.NotNull(finalState["Parameters"]);
+            Assert.NotNull(finalState["Azure"]);
+            Assert.Equal("value1", finalState["Parameters"]!["param1"]!.ToString());
+            Assert.Equal("sub-123", finalState["Azure"]!["SubscriptionId"]!.ToString());
+        }
+        finally
+        {
+            if (Directory.Exists(tempDir))
+            {
+                Directory.Delete(tempDir, true);
+            }
+        }
+    }
+
+    [Fact]
+    public async Task SaveStateAsync_PreservesExistingKeysNotInNewState()
+    {
+        // Arrange
+        var tempDir = Path.Combine(Path.GetTempPath(), Guid.NewGuid().ToString());
+        Directory.CreateDirectory(tempDir);
+        var secretsFile = Path.Combine(tempDir, "secrets.json");
+
+        try
+        {
+            // Create initial state with multiple keys
+            var initialState = new JsonObject
+            {
+                ["Key1"] = "value1",
+                ["Key2"] = "value2",
+                ["Key3"] = "value3"
+            };
+            await File.WriteAllTextAsync(secretsFile, initialState.ToJsonString());
+
+            // New state only updates Key2 and adds Key4
+            var newState = new JsonObject
+            {
+                ["Key2"] = "updated-value2",
+                ["Key4"] = "value4"
+            };
+
+            // Simulate merge
+            var loadedState = JsonNode.Parse(await File.ReadAllTextAsync(secretsFile))!.AsObject();
+            foreach (var kvp in newState)
+            {
+                loadedState[kvp.Key] = kvp.Value?.DeepClone();
+            }
+
+            // Act
+            await File.WriteAllTextAsync(secretsFile, loadedState.ToJsonString());
+
+            // Assert - All keys should be present with correct values
+            var finalState = JsonNode.Parse(await File.ReadAllTextAsync(secretsFile))!.AsObject();
+            Assert.Equal(4, finalState.Count);
+            Assert.Equal("value1", finalState["Key1"]!.ToString());
+            Assert.Equal("updated-value2", finalState["Key2"]!.ToString());
+            Assert.Equal("value3", finalState["Key3"]!.ToString());
+            Assert.Equal("value4", finalState["Key4"]!.ToString());
+        }
+        finally
+        {
+            if (Directory.Exists(tempDir))
+            {
+                Directory.Delete(tempDir, true);
+            }
+        }
+    }
+
+    [Fact]
+    public async Task SaveStateAsync_OverwritesExistingKeysWithNewValues()
+    {
+        // Arrange
+        var tempDir = Path.Combine(Path.GetTempPath(), Guid.NewGuid().ToString());
+        Directory.CreateDirectory(tempDir);
+        var secretsFile = Path.Combine(tempDir, "secrets.json");
+
+        try
+        {
+            // Create initial state
+            var initialState = new JsonObject
+            {
+                ["Azure"] = new JsonObject
+                {
+                    ["SubscriptionId"] = "old-sub-id",
+                    ["Tenant"] = "old-tenant"
+                }
+            };
+            await File.WriteAllTextAsync(secretsFile, initialState.ToJsonString());
+
+            // New state with updated Azure data
+            var newState = new JsonObject
+            {
+                ["Azure"] = new JsonObject
+                {
+                    ["SubscriptionId"] = "new-sub-id",
+                    ["Tenant"] = "new-tenant"
+                }
+            };
+
+            // Simulate merge
+            var loadedState = JsonNode.Parse(await File.ReadAllTextAsync(secretsFile))!.AsObject();
+            foreach (var kvp in newState)
+            {
+                loadedState[kvp.Key] = kvp.Value?.DeepClone();
+            }
+
+            // Act
+            await File.WriteAllTextAsync(secretsFile, loadedState.ToJsonString());
+
+            // Assert - Azure values should be updated
+            var finalState = JsonNode.Parse(await File.ReadAllTextAsync(secretsFile))!.AsObject();
+            Assert.Equal("new-sub-id", finalState["Azure"]!["SubscriptionId"]!.ToString());
+            Assert.Equal("new-tenant", finalState["Azure"]!["Tenant"]!.ToString());
+        }
+        finally
+        {
+            if (Directory.Exists(tempDir))
+            {
+                Directory.Delete(tempDir, true);
+            }
+        }
+    }
 }
\ No newline at end of file