diff --git a/e2e-tests/cypress/tests/integration/channels/plugins/link_tooltip_spec.js b/e2e-tests/cypress/tests/integration/channels/plugins/link_tooltip_spec.js
index 58a65272b9c..4f95f412f43 100644
--- a/e2e-tests/cypress/tests/integration/channels/plugins/link_tooltip_spec.js
+++ b/e2e-tests/cypress/tests/integration/channels/plugins/link_tooltip_spec.js
@@ -17,18 +17,10 @@ describe('Link tooltips', () => {
         cy.shouldNotRunOnCloudEdition();
         cy.shouldHavePluginUploadEnabled();
 
-        // # Set plugin settings, including demo plugin defaults so that
-        // OnConfigurationChange can create the demo user with a valid email
+        // # Set plugin settings
         const newSettings = {
             PluginSettings: {
                 Enable: true,
-                Plugins: {
-                    [demoPlugin.id]: {
-                        channelname: 'demo_plugin',
-                        username: 'demo_plugin',
-                        lastname: 'Plugin User',
-                    },
-                },
             },
             ServiceSettings: {
                 EnableGifPicker: true,
diff --git a/server/channels/app/plugin_api.go b/server/channels/app/plugin_api.go
index de29ba9f534..71d025efabb 100644
--- a/server/channels/app/plugin_api.go
+++ b/server/channels/app/plugin_api.go
@@ -55,6 +55,11 @@ func (api *PluginAPI) LoadPluginConfiguration(dest any) error {
 		for _, setting := range api.manifest.SettingsSchema.Settings {
 			finalConfig[strings.ToLower(setting.Key)] = setting.Default
 		}
+		for _, section := range api.manifest.SettingsSchema.Sections {
+			for _, setting := range section.Settings {
+				finalConfig[strings.ToLower(setting.Key)] = setting.Default
+			}
+		}
 	}
 
 	// If we have settings given we override the defaults with them
diff --git a/server/channels/app/plugin_api_test.go b/server/channels/app/plugin_api_test.go
index 8903b2bc2bc..4688a231bfc 100644
--- a/server/channels/app/plugin_api_test.go
+++ b/server/channels/app/plugin_api_test.go
@@ -982,6 +982,101 @@ func TestPluginAPILoadPluginConfigurationDefaults(t *testing.T) {
 	require.NoError(t, err)
 }
 
+func TestPluginAPILoadPluginConfigurationDefaultsFromSections(t *testing.T) {
+	mainHelper.Parallel(t)
+	th := Setup(t)
+
+	var pluginJson map[string]any
+	err := json.Unmarshal([]byte(`{"mysectionstringsetting": "override"}`), &pluginJson)
+	require.NoError(t, err)
+
+	th.App.UpdateConfig(func(cfg *model.Config) {
+		cfg.PluginSettings.Plugins["testsectiondefaults"] = pluginJson
+	})
+
+	manifest := &model.Manifest{
+		Id: "testsectiondefaults",
+		SettingsSchema: &model.PluginSettingsSchema{
+			Sections: []*model.PluginSettingsSection{
+				{
+					Key: "section1",
+					Settings: []*model.PluginSetting{
+						{Key: "MySectionStringSetting", Type: "text", Default: "notthis"},
+						{Key: "MySectionIntSetting", Type: "text", Default: float64(42)},
+						{Key: "MySectionBoolSetting", Type: "bool", Default: true},
+					},
+				},
+			},
+		},
+	}
+
+	api := NewPluginAPI(th.App, th.Context, manifest)
+
+	var dest struct {
+		MySectionStringSetting string
+		MySectionIntSetting    int
+		MySectionBoolSetting   bool
+	}
+	err = api.LoadPluginConfiguration(&dest)
+	require.NoError(t, err)
+
+	assert.Equal(t, "override", dest.MySectionStringSetting) // saved config overrides default
+	assert.Equal(t, 42, dest.MySectionIntSetting)            // default applied from section
+	assert.True(t, dest.MySectionBoolSetting)                // default applied from section
+}
+
+func TestPluginAPILoadPluginConfigurationDefaultsMixed(t *testing.T) {
+	mainHelper.Parallel(t)
+	th := Setup(t)
+
+	var pluginJson map[string]any
+	err := json.Unmarshal([]byte(`{"toplevelsetting": "saved_value"}`), &pluginJson)
+	require.NoError(t, err)
+
+	th.App.UpdateConfig(func(cfg *model.Config) {
+		cfg.PluginSettings.Plugins["testmixeddefaults"] = pluginJson
+	})
+
+	manifest := &model.Manifest{
+		Id: "testmixeddefaults",
+		SettingsSchema: &model.PluginSettingsSchema{
+			Settings: []*model.PluginSetting{
+				{Key: "TopLevelSetting", Type: "text", Default: "top_default"},
+				{Key: "TopLevelBool", Type: "bool", Default: true},
+			},
+			Sections: []*model.PluginSettingsSection{
+				{
+					Key: "section1",
+					Settings: []*model.PluginSetting{
+						{Key: "SectionSetting", Type: "text", Default: "section_default"},
+						{Key: "SectionInt", Type: "text", Default: float64(99)},
+					},
+				},
+			},
+		},
+	}
+
+	api := NewPluginAPI(th.App, th.Context, manifest)
+
+	var dest struct {
+		TopLevelSetting string
+		TopLevelBool    bool
+		SectionSetting  string
+		SectionInt      int
+	}
+	err = api.LoadPluginConfiguration(&dest)
+	require.NoError(t, err)
+
+	// Top-level: saved config overrides default
+	assert.Equal(t, "saved_value", dest.TopLevelSetting)
+	// Top-level: default applied
+	assert.True(t, dest.TopLevelBool)
+	// Section: default applied
+	assert.Equal(t, "section_default", dest.SectionSetting)
+	// Section: default applied
+	assert.Equal(t, 99, dest.SectionInt)
+}
+
 func TestPluginAPIGetPlugins(t *testing.T) {
 	mainHelper.Parallel(t)
 	th := Setup(t)