diff --git a/core/modules/layout_builder/layout_builder.module b/core/modules/layout_builder/layout_builder.module
index 76ec53433d..bda807a1f5 100644
--- a/core/modules/layout_builder/layout_builder.module
+++ b/core/modules/layout_builder/layout_builder.module
@@ -134,3 +134,12 @@ function layout_builder_module_implements_alter(&$implementations, $hook) {
     $implementations['layout_builder'] = $group;
   }
 }
+
+/**
+ * Implements hook_layout_builder_section_storage_alter().
+ */
+function layout_builder_layout_builder_section_storage_alter(array &$definitions) {
+  /** @var \Drupal\layout_builder\SectionStorage\SectionStorageDefinition[] $definitions */
+  $definitions['overrides']->getContextDefinition('entity')
+    ->addConstraint('EntityHasField', 'layout_builder__layout');
+}
diff --git a/core/modules/layout_builder/layout_builder.module.rej b/core/modules/layout_builder/layout_builder.module.rej
new file mode 100644
index 0000000000..49cd3cb856
--- /dev/null
+++ b/core/modules/layout_builder/layout_builder.module.rej
@@ -0,0 +1,14 @@
+diff a/core/modules/layout_builder/layout_builder.module b/core/modules/layout_builder/layout_builder.module	(rejected hunks)
+@@ -202,3 +202,12 @@ function layout_builder_block_content_access(EntityInterface $entity, $operation
+   }
+   return AccessResult::forbidden();
+ }
++
++/**
+++ * Implements hook_layout_builder_section_storage_alter().
+++ */
++function layout_builder_layout_builder_section_storage_alter(array &$definitions) {
++  /** @var \Drupal\layout_builder\SectionStorage\SectionStorageDefinition[] $definitions */
++  $definitions['overrides']->getContextDefinition('entity')
++    ->addConstraint('EntityHasField', 'layout_builder__layout');
++}
diff --git a/core/modules/layout_builder/src/Annotation/SectionStorage.php b/core/modules/layout_builder/src/Annotation/SectionStorage.php
index 42f4a47fe6..e84fbaad2e 100644
--- a/core/modules/layout_builder/src/Annotation/SectionStorage.php
+++ b/core/modules/layout_builder/src/Annotation/SectionStorage.php
@@ -22,6 +22,13 @@ class SectionStorage extends Plugin {
    */
   public $id;
 
+  /**
+   * Any required context definitions.
+   *
+   * @var array
+   */
+  public $context = [];
+
   /**
    * {@inheritdoc}
    */
diff --git a/core/modules/layout_builder/src/Entity/LayoutBuilderEntityViewDisplay.php b/core/modules/layout_builder/src/Entity/LayoutBuilderEntityViewDisplay.php
index 78ff430b00..305e0a8f53 100644
--- a/core/modules/layout_builder/src/Entity/LayoutBuilderEntityViewDisplay.php
+++ b/core/modules/layout_builder/src/Entity/LayoutBuilderEntityViewDisplay.php
@@ -5,6 +5,8 @@
 use Drupal\Core\Entity\Entity\EntityViewDisplay as BaseEntityViewDisplay;
 use Drupal\Core\Entity\EntityStorageInterface;
 use Drupal\Core\Entity\FieldableEntityInterface;
+use Drupal\Core\Plugin\Context\Context;
+use Drupal\Core\Plugin\Context\ContextDefinition;
 use Drupal\Core\Plugin\Context\EntityContext;
 use Drupal\Core\StringTranslation\TranslatableMarkup;
 use Drupal\field\Entity\FieldConfig;
@@ -239,11 +241,27 @@ public function buildMultiple(array $entities) {
    *   The sections.
    */
   protected function getRuntimeSections(FieldableEntityInterface $entity) {
-    if ($this->isOverridable() && !$entity->get('layout_builder__layout')->isEmpty()) {
-      return $entity->get('layout_builder__layout')->getSections();
-    }
+    if ($this->isOverridable()) {
+      $contexts = [
+        'entity' => new Context(ContextDefinition::create('entity'), $entity),
+      ];
+
+      /** @var \Drupal\layout_builder\SectionStorage\SectionStorageManagerInterface $storage_manager */
+      $storage_manager = \Drupal::service('plugin.manager.layout_builder.section_storage');
+
+      $definitions = $storage_manager->getDefinitionsForContexts($contexts);
+      if ($definitions) {
+        $storage_type = key($definitions);
 
-    return $this->getSections();
+        $storage = $storage_manager->loadEmpty($storage_type);
+        $storage->setContext('entity', $contexts['entity']);
+        $section_list = $storage->getSectionListFromContext();
+      }
+    }
+    if (empty($section_list) || count($section_list) === 0) {
+      $section_list = $this;
+    }
+    return $section_list->getSections();
   }
 
   /**
diff --git a/core/modules/layout_builder/src/Plugin/SectionStorage/DefaultsSectionStorage.php b/core/modules/layout_builder/src/Plugin/SectionStorage/DefaultsSectionStorage.php
index 6fab11996b..623bd01252 100644
--- a/core/modules/layout_builder/src/Plugin/SectionStorage/DefaultsSectionStorage.php
+++ b/core/modules/layout_builder/src/Plugin/SectionStorage/DefaultsSectionStorage.php
@@ -25,6 +25,9 @@
  *
  * @SectionStorage(
  *   id = "defaults",
+ *   context = {
+ *     "entity_view_display" = @ContextDefinition("entity:entity_view_display"),
+ *   }
  * )
  *
  * @internal
@@ -249,6 +252,13 @@ public function getSectionListFromId($id) {
     return $display;
   }
 
+  /**
+   * {@inheritdoc}
+   */
+  public function getSectionListFromContext() {
+    return $this->getContextValue('entity_view_display');
+  }
+
   /**
    * {@inheritdoc}
    */
diff --git a/core/modules/layout_builder/src/Plugin/SectionStorage/OverridesSectionStorage.php b/core/modules/layout_builder/src/Plugin/SectionStorage/OverridesSectionStorage.php
index 3a92ee63fa..b13deb0cfe 100644
--- a/core/modules/layout_builder/src/Plugin/SectionStorage/OverridesSectionStorage.php
+++ b/core/modules/layout_builder/src/Plugin/SectionStorage/OverridesSectionStorage.php
@@ -23,6 +23,9 @@
  *
  * @SectionStorage(
  *   id = "overrides",
+ *   context = {
+ *     "entity" = @ContextDefinition("entity"),
+ *   }
  * )
  *
  * @internal
@@ -134,6 +137,13 @@ public function getSectionListFromId($id) {
     throw new \InvalidArgumentException(sprintf('The "%s" ID for the "%s" section storage type is invalid', $id, $this->getStorageType()));
   }
 
+  /**
+   * {@inheritdoc}
+   */
+  public function getSectionListFromContext() {
+    return $this->getContextValue('entity')->get('layout_builder__layout');
+  }
+
   /**
    * {@inheritdoc}
    */
diff --git a/core/modules/layout_builder/src/Plugin/SectionStorage/SectionStorageBase.php b/core/modules/layout_builder/src/Plugin/SectionStorage/SectionStorageBase.php
index c419060c45..ae6569cb33 100644
--- a/core/modules/layout_builder/src/Plugin/SectionStorage/SectionStorageBase.php
+++ b/core/modules/layout_builder/src/Plugin/SectionStorage/SectionStorageBase.php
@@ -2,7 +2,7 @@
 
 namespace Drupal\layout_builder\Plugin\SectionStorage;
 
-use Drupal\Core\Plugin\PluginBase;
+use Drupal\Core\Plugin\ContextAwarePluginBase;
 use Drupal\layout_builder\Routing\LayoutBuilderRoutesTrait;
 use Drupal\layout_builder\Section;
 use Drupal\layout_builder\SectionListInterface;
@@ -16,7 +16,7 @@
  *   experimental modules and development releases of contributed modules.
  *   See https://www.drupal.org/core/experimental for more information.
  */
-abstract class SectionStorageBase extends PluginBase implements SectionStorageInterface {
+abstract class SectionStorageBase extends ContextAwarePluginBase implements SectionStorageInterface {
 
   use LayoutBuilderRoutesTrait;
 
@@ -103,4 +103,22 @@ public function removeSection($delta) {
     return $this;
   }
 
+  /**
+   * {@inheritdoc}
+   *
+   * @todo Remove after https://www.drupal.org/project/drupal/issues/2982626.
+   */
+  public function getContextDefinition($name) {
+    return $this->getPluginDefinition()->getContextDefinition($name);
+  }
+
+  /**
+   * {@inheritdoc}
+   *
+   * @todo Remove after https://www.drupal.org/project/drupal/issues/2982626.
+   */
+  public function getContextDefinitions() {
+    return $this->getPluginDefinition()->getContextDefinitions();
+  }
+
 }
diff --git a/core/modules/layout_builder/src/SectionStorage/SectionStorageDefinition.php b/core/modules/layout_builder/src/SectionStorage/SectionStorageDefinition.php
index 61b975a471..673cfb31fc 100644
--- a/core/modules/layout_builder/src/SectionStorage/SectionStorageDefinition.php
+++ b/core/modules/layout_builder/src/SectionStorage/SectionStorageDefinition.php
@@ -2,6 +2,8 @@
 
 namespace Drupal\layout_builder\SectionStorage;
 
+use Drupal\Component\Plugin\Definition\ContextAwarePluginDefinitionInterface;
+use Drupal\Component\Plugin\Definition\ContextAwarePluginDefinitionTrait;
 use Drupal\Component\Plugin\Definition\PluginDefinition;
 
 /**
@@ -12,7 +14,9 @@
  *   experimental modules and development releases of contributed modules.
  *   See https://www.drupal.org/core/experimental for more information.
  */
-class SectionStorageDefinition extends PluginDefinition {
+class SectionStorageDefinition extends PluginDefinition implements ContextAwarePluginDefinitionInterface {
+
+  use ContextAwarePluginDefinitionTrait;
 
   /**
    * Any additional properties and values.
@@ -28,6 +32,13 @@ class SectionStorageDefinition extends PluginDefinition {
    *   An array of values from the annotation.
    */
   public function __construct(array $definition = []) {
+    if (isset($definition['context'])) {
+      foreach ($definition['context'] as $name => $context_definition) {
+        $this->addContextDefinition($name, $context_definition);
+      }
+      unset($definition['context']);
+    }
+
     foreach ($definition as $property => $value) {
       $this->set($property, $value);
     }
diff --git a/core/modules/layout_builder/src/SectionStorage/SectionStorageManager.php b/core/modules/layout_builder/src/SectionStorage/SectionStorageManager.php
index 18147cd1d8..8f24b06cb0 100644
--- a/core/modules/layout_builder/src/SectionStorage/SectionStorageManager.php
+++ b/core/modules/layout_builder/src/SectionStorage/SectionStorageManager.php
@@ -4,6 +4,7 @@
 
 use Drupal\Core\Cache\CacheBackendInterface;
 use Drupal\Core\Extension\ModuleHandlerInterface;
+use Drupal\Core\Plugin\Context\ContextAwarePluginManagerTrait;
 use Drupal\Core\Plugin\DefaultPluginManager;
 use Drupal\layout_builder\Annotation\SectionStorage;
 use Drupal\layout_builder\SectionStorageInterface;
@@ -18,6 +19,8 @@
  */
 class SectionStorageManager extends DefaultPluginManager implements SectionStorageManagerInterface {
 
+  use ContextAwarePluginManagerTrait;
+
   /**
    * Constructs a new SectionStorageManager object.
    *
diff --git a/core/modules/layout_builder/src/SectionStorage/SectionStorageManagerInterface.php b/core/modules/layout_builder/src/SectionStorage/SectionStorageManagerInterface.php
index 3b269fcbba..8cf53b620a 100644
--- a/core/modules/layout_builder/src/SectionStorage/SectionStorageManagerInterface.php
+++ b/core/modules/layout_builder/src/SectionStorage/SectionStorageManagerInterface.php
@@ -2,7 +2,7 @@
 
 namespace Drupal\layout_builder\SectionStorage;
 
-use Drupal\Component\Plugin\Discovery\DiscoveryInterface;
+use Drupal\Core\Plugin\Context\ContextAwarePluginManagerInterface;
 
 /**
  * Provides the interface for a plugin manager of section storage types.
@@ -12,7 +12,7 @@
  *   experimental modules and development releases of contributed modules.
  *   See https://www.drupal.org/core/experimental for more information.
  */
-interface SectionStorageManagerInterface extends DiscoveryInterface {
+interface SectionStorageManagerInterface extends ContextAwarePluginManagerInterface {
 
   /**
    * Loads a section storage with no associated section list.
diff --git a/core/modules/layout_builder/src/SectionStorageInterface.php b/core/modules/layout_builder/src/SectionStorageInterface.php
index 90ce9072fd..9a1aa61934 100644
--- a/core/modules/layout_builder/src/SectionStorageInterface.php
+++ b/core/modules/layout_builder/src/SectionStorageInterface.php
@@ -2,8 +2,8 @@
 
 namespace Drupal\layout_builder;
 
-use Drupal\Component\Plugin\PluginInspectionInterface;
 use Drupal\Core\Access\AccessibleInterface;
+use Drupal\Core\Plugin\ContextAwarePluginInterface;
 use Symfony\Component\Routing\RouteCollection;
 
 /**
@@ -14,7 +14,7 @@
  *   experimental modules and development releases of contributed modules.
  *   See https://www.drupal.org/core/experimental for more information.
  */
-interface SectionStorageInterface extends SectionListInterface, PluginInspectionInterface, AccessibleInterface {
+interface SectionStorageInterface extends SectionListInterface, ContextAwarePluginInterface, AccessibleInterface {
 
   /**
    * Returns an identifier for this storage.
@@ -64,6 +64,17 @@ public function setSectionList(SectionListInterface $section_list);
    */
   public function getSectionListFromId($id);
 
+  /**
+   * Derives the section list from the available context.
+   *
+   * @return \Drupal\layout_builder\SectionListInterface
+   *   The section list.
+   *
+   * @internal
+   *   This should only be called during section storage instantiation.
+   */
+  public function getSectionListFromContext();
+
   /**
    * Provides the routes needed for Layout Builder UI.
    *
diff --git a/core/modules/layout_builder/tests/modules/layout_builder_test/layout_builder_test.module b/core/modules/layout_builder/tests/modules/layout_builder_test/layout_builder_test.module
index e7d310a6cb..38b66f557d 100644
--- a/core/modules/layout_builder/tests/modules/layout_builder_test/layout_builder_test.module
+++ b/core/modules/layout_builder/tests/modules/layout_builder_test/layout_builder_test.module
@@ -7,6 +7,7 @@
 
 use Drupal\Core\Entity\Display\EntityViewDisplayInterface;
 use Drupal\Core\Entity\EntityInterface;
+use Drupal\layout_builder_test\Plugin\SectionStorage\OverridesSectionStorage;
 
 /**
  * Implements hook_plugin_filter_TYPE__CONSUMER_alter().
@@ -58,3 +59,11 @@ function layout_builder_test_node_view(array &$build, EntityInterface $entity, E
     ];
   }
 }
+
+/**
+ * Implements hook_layout_builder_section_storage_alter().
+ */
+function layout_builder_test_layout_builder_section_storage_alter(array &$storages) {
+  /** @var \Drupal\layout_builder\SectionStorage\SectionStorageDefinition[] $storages */
+  $storages['overrides']->setClass(OverridesSectionStorage::class);
+}
diff --git a/core/modules/layout_builder/tests/modules/layout_builder_test/src/Plugin/SectionStorage/OverridesSectionStorage.php b/core/modules/layout_builder/tests/modules/layout_builder_test/src/Plugin/SectionStorage/OverridesSectionStorage.php
new file mode 100644
index 0000000000..f6d492d5b8
--- /dev/null
+++ b/core/modules/layout_builder/tests/modules/layout_builder_test/src/Plugin/SectionStorage/OverridesSectionStorage.php
@@ -0,0 +1,17 @@
+<?php
+
+namespace Drupal\layout_builder_test\Plugin\SectionStorage;
+
+use Drupal\layout_builder\Plugin\SectionStorage\OverridesSectionStorage as BaseOverridesSectionStorage;
+
+class OverridesSectionStorage extends BaseOverridesSectionStorage {
+
+  /**
+   * {@inheritdoc}
+   */
+  public function getSectionListFromContext() {
+    \Drupal::state()->set('layout_builder_test_context_applied', TRUE);
+    return parent::getSectionListFromContext();
+  }
+
+}
diff --git a/core/modules/layout_builder/tests/src/Functional/LayoutBuilderTest.php b/core/modules/layout_builder/tests/src/Functional/LayoutBuilderTest.php
index d39c7e673f..c7a3c5cdc9 100644
--- a/core/modules/layout_builder/tests/src/Functional/LayoutBuilderTest.php
+++ b/core/modules/layout_builder/tests/src/Functional/LayoutBuilderTest.php
@@ -2,6 +2,7 @@
 
 namespace Drupal\Tests\layout_builder\Functional;
 
+use Drupal\layout_builder\Entity\LayoutBuilderEntityViewDisplay;
 use Drupal\node\Entity\Node;
 use Drupal\Tests\BrowserTestBase;
 use Drupal\views\Entity\View;
@@ -444,6 +445,27 @@ public function testDeletedView() {
     $assert_session->pageTextNotContains('Test Block View');
   }
 
+  /**
+   * Tests that section loading is delegated to plugins during rendering.
+   */
+  public function testRenderByContextualPluginDelegate() {
+    $state_key = 'layout_builder_test_context_applied';
+    /** @var \Drupal\Core\State\StateInterface $state */
+    $state = $this->container->get('state');
+
+    $this->drupalGet('node/1');
+    $this->assertEmpty($state->get($state_key));
+
+    entity_get_display('node', 'bundle_with_section_field', 'full')
+      ->enableLayoutBuilder()
+      ->setOverridable()
+      ->save();
+
+    $this->getSession()->reload();
+    $state->resetCache();
+    $this->assertTrue($state->get($state_key));
+  }
+
   /**
    * Asserts that a text string only appears once on the page.
    *
@@ -451,7 +473,9 @@ public function testDeletedView() {
    *   The string to look for.
    */
   protected function assertTextAppearsOnce($needle) {
-    $this->assertEquals(1, substr_count($this->getSession()->getPage()->getContent(), $needle), "'$needle' only appears once on the page.");
+    $this->assertEquals(1, substr_count($this->getSession()
+      ->getPage()
+      ->getContent(), $needle), "'$needle' only appears once on the page.");
   }
 
 }