diff --git a/platform/platform-impl/src/com/intellij/openapi/wm/impl/WindowButtonsConfiguration.kt b/platform/platform-impl/src/com/intellij/openapi/wm/impl/WindowButtonsConfiguration.kt
index 678056c0272c..6e0e0abc5582 100644
--- a/platform/platform-impl/src/com/intellij/openapi/wm/impl/WindowButtonsConfiguration.kt
+++ b/platform/platform-impl/src/com/intellij/openapi/wm/impl/WindowButtonsConfiguration.kt
@@ -1,19 +1,23 @@
 // Copyright 2000-2024 JetBrains s.r.o. and contributors. Use of this source code is governed by the Apache 2.0 license.
 @file:ApiStatus.Internal
+
 package com.intellij.openapi.wm.impl
 
-import com.intellij.ide.AppLifecycleListener
 import com.intellij.openapi.components.PersistentStateComponent
 import com.intellij.openapi.components.State
 import com.intellij.openapi.components.Storage
 import com.intellij.openapi.components.StoragePathMacros
 import com.intellij.openapi.components.service
+import com.intellij.openapi.diagnostic.thisLogger
 import com.intellij.openapi.util.SystemInfoRt
-import com.intellij.openapi.util.registry.Registry
+import com.intellij.openapi.util.registry.RegistryManager
+import com.intellij.util.concurrency.ThreadingAssertions
+import kotlinx.coroutines.CoroutineName
 import kotlinx.coroutines.CoroutineScope
 import kotlinx.coroutines.flow.MutableStateFlow
 import kotlinx.coroutines.flow.StateFlow
 import kotlinx.coroutines.flow.asStateFlow
+import kotlinx.coroutines.flow.update
 import kotlinx.coroutines.launch
 import org.jetbrains.annotations.ApiStatus
 
@@ -22,7 +26,7 @@ import org.jetbrains.annotations.ApiStatus
  */
 @ApiStatus.Internal
 @State(name = "WindowButtonsConfiguration", storages = [Storage(StoragePathMacros.CACHE_FILE)])
-class WindowButtonsConfiguration(private val scope: CoroutineScope) : PersistentStateComponent<WindowButtonsConfiguration.State?> {
+class WindowButtonsConfiguration(scope: CoroutineScope) : PersistentStateComponent<WindowButtonsConfiguration.State?> {
   enum class WindowButton {
     MINIMIZE,
     MAXIMIZE,
@@ -32,6 +36,9 @@ class WindowButtonsConfiguration(private val scope: CoroutineScope) : Persistent
   companion object {
     fun getInstance(): WindowButtonsConfiguration? = if (isSupported()) service<WindowButtonsConfiguration>() else null
 
+    private val log = thisLogger()
+    private const val WINDOW_BUTTONS_CONFIG_KEY = "ide.linux.window.buttons.config"
+
     private fun isSupported(): Boolean {
       return SystemInfoRt.isLinux
     }
@@ -40,35 +47,55 @@ class WindowButtonsConfiguration(private val scope: CoroutineScope) : Persistent
   private var mutableStateFlow = MutableStateFlow<State?>(null)
   val stateFlow: StateFlow<State?> = mutableStateFlow.asStateFlow()
 
+  init {
+    if (isSupported()) {
+      scope.launch(CoroutineName("WindowButtonsConfiguration")) {
+        val registryManager = RegistryManager.getInstanceAsync()
+        registryManager.awaitRegistryLoad()
+
+        var state = loadStateFromRegistry(registryManager) ?: loadStateFromOs()
+        mutableStateFlow.update { state }
+      }
+    }
+  }
+
   override fun getState(): State? {
     return mutableStateFlow.value
   }
 
   override fun loadState(state: State) {
-    mutableStateFlow.value = state
-    scheduleUpdateFromOs()
-  }
-
-  override fun noStateLoaded() {
-    scheduleUpdateFromOs()
-  }
-
-  fun scheduleUpdateFromOs(customConfig: String? = null) {
-    scope.launch {
-      loadStateFromOs(customConfig)
+    mutableStateFlow.update { currentState ->
+      // The saved state is used only for caching, the actual computed state takes priority.
+      // Normally the state isn't computed yet, unless loadState is called when the service is already up and running.
+      // This is possible, according to the API docs, but only if the files are modified when the IDE is running.
+      // In this case we definitely don't want to pick up the modified value, as the sources of truth are the OS and the registry.
+      currentState ?: state
     }
   }
 
-  private fun loadStateFromOs(customConfig: String?) {
-    var windowButtonsState: State? = null
-
-    if (isSupported()) {
-      val config = if (customConfig.isNullOrBlank()) X11UiUtil.getWindowButtonsConfig() else customConfig
-      if (config != null) {
-        windowButtonsState = parseFromString(config)
-      }
+  private fun loadStateFromRegistry(registryManager: RegistryManager): State? {
+    val value = registryManager.stringValue(WINDOW_BUTTONS_CONFIG_KEY)
+    if (value.isNullOrEmpty()) {
+      return null
     }
-    mutableStateFlow.value = windowButtonsState
+
+    val result = parseFromString(value)
+    if (result == null) {
+      log.warn("Failed to parse '$WINDOW_BUTTONS_CONFIG_KEY' registry value: $value")
+    }
+
+    return result
+  }
+
+  private fun loadStateFromOs(): State? {
+    ThreadingAssertions.assertBackgroundThread()
+
+    val config = X11UiUtil.getWindowButtonsConfig() ?: return null
+    val result = parseFromString(config)
+    if (result == null) {
+      log.warn("Failed to parse OS window buttons config: $config")
+    }
+    return result
   }
 
   class State {
@@ -113,10 +140,3 @@ private fun stringsToWindowButtons(strings: List<String>): List<WindowButtonsCon
     }
   }
 }
-
-internal class WindowButtonsAppLifecycleListener : AppLifecycleListener {
-
-  override fun appStarted() {
-    WindowButtonsConfiguration.getInstance()?.scheduleUpdateFromOs(Registry.stringValue("ide.linux.window.buttons.config"))
-  }
-}
\ No newline at end of file
diff --git a/platform/platform-resources/src/META-INF/PlatformExtensions.xml b/platform/platform-resources/src/META-INF/PlatformExtensions.xml
index 3f169d1bf8cf..3063c4b276f4 100644
--- a/platform/platform-resources/src/META-INF/PlatformExtensions.xml
+++ b/platform/platform-resources/src/META-INF/PlatformExtensions.xml
@@ -2114,7 +2114,6 @@
               topic="com.intellij.ide.ui.UISettingsListener"/>
     <listener class="com.intellij.ui.MacCustomAppIconStartupService" topic="com.intellij.ide.AppLifecycleListener"/>
     <listener class="com.intellij.openapi.editor.actions.ResetFontSizeAppInitListener" topic="com.intellij.ide.AppLifecycleListener"/>
-    <listener class="com.intellij.openapi.wm.impl.WindowButtonsAppLifecycleListener" topic="com.intellij.ide.AppLifecycleListener" os="linux"/>
 
     <listener class="com.intellij.ui.ExperimentalUiAppLifecycleListener" topic="com.intellij.ide.AppLifecycleListener"/>
     <listener class="com.intellij.ide.ui.laf.LafAndEditorColorSchemeDynamicPluginListener"
diff --git a/platform/util/resources/misc/registry.properties b/platform/util/resources/misc/registry.properties
index 4bcb23d307ea..025483e7a8b3 100644
--- a/platform/util/resources/misc/registry.properties
+++ b/platform/util/resources/misc/registry.properties
@@ -1886,6 +1886,7 @@ ide.linux.use.undecorated.border.restartRequired=true
 
 ide.linux.window.buttons.config=
 ide.linux.window.buttons.config.description=Custom window buttons configuration, which is get by `gsettings get org.gnome.desktop.wm.preferences button-layout` command by default. Format should be similar to the command result, e.g. `:minimize,maximize,close`
+ide.linux.window.buttons.config.restartRequired=true
 
 ide.tree.large.model.allowed=false
 ide.tree.large.model.allowed.description=Allows using FixedHeightLayoutCache if setLargeModel(true)