diff --git a/app/models/custom_field_section.rb b/app/models/custom_field_section.rb
index 2eba38951e3..84f9db4f3d1 100644
--- a/app/models/custom_field_section.rb
+++ b/app/models/custom_field_section.rb
@@ -31,7 +31,7 @@
 class CustomFieldSection < ApplicationRecord
   OVERVIEW__SIDEBAR_KEY = "sidebar"
   OVERVIEW__MAIN_AREA_KEY = "main_area"
-  DEFAULT_OVERVIEW_KEY = OVERVIEW__SIDEBAR_KEY.freeze
+  DEFAULT_OVERVIEW_KEY = OVERVIEW__SIDEBAR_KEY
 
   acts_as_list scope: [:type]
 
@@ -39,7 +39,7 @@ class CustomFieldSection < ApplicationRecord
 
   default_scope { order(:position) }
 
-  store_attribute :display_representation, :overview, :string
+  store_attribute :display_representation, :overview, :string, default: DEFAULT_OVERVIEW_KEY
 
   def shown_in_overview_sidebar?
     overview == OVERVIEW__SIDEBAR_KEY
diff --git a/db/migrate/20260304164536_fix_empty_display_representation_on_cf_sections.rb b/db/migrate/20260304164536_fix_empty_display_representation_on_cf_sections.rb
new file mode 100644
index 00000000000..01fb839050b
--- /dev/null
+++ b/db/migrate/20260304164536_fix_empty_display_representation_on_cf_sections.rb
@@ -0,0 +1,44 @@
+# frozen_string_literal: true
+
+#-- copyright
+# OpenProject is an open source project management software.
+# Copyright (C) the OpenProject GmbH
+#
+# This program is free software; you can redistribute it and/or
+# modify it under the terms of the GNU General Public License version 3.
+#
+# OpenProject is a fork of ChiliProject, which is a fork of Redmine. The copyright follows:
+# Copyright (C) 2006-2013 Jean-Philippe Lang
+# Copyright (C) 2010-2013 the ChiliProject Team
+#
+# This program is free software; you can redistribute it and/or
+# modify it under the terms of the GNU General Public License
+# as published by the Free Software Foundation; either version 2
+# of the License, or (at your option) any later version.
+#
+# This program is distributed in the hope that it will be useful,
+# but WITHOUT ANY WARRANTY; without even the implied warranty of
+# MERCHANTABILITY or FITNESS FOR A PARTICULAR PURPOSE.  See the
+# GNU General Public License for more details.
+#
+# You should have received a copy of the GNU General Public License
+# along with this program; if not, write to the Free Software
+# Foundation, Inc., 51 Franklin Street, Fifth Floor, Boston, MA  02110-1301, USA.
+#
+# See COPYRIGHT and LICENSE files for more details.
+#++
+
+class FixEmptyDisplayRepresentationOnCfSections < ActiveRecord::Migration[8.1]
+  def up
+    execute <<~SQL.squish
+      UPDATE custom_field_sections
+      SET display_representation = '{"overview": "#{CustomFieldSection::DEFAULT_OVERVIEW_KEY}"}'
+      WHERE display_representation = '{}'
+    SQL
+  end
+
+  def down
+    # No rollback: we cannot distinguish sections that originally had {}
+    # from ones that legitimately had the default value set.
+  end
+end
diff --git a/spec/models/custom_field_section_spec.rb b/spec/models/custom_field_section_spec.rb
new file mode 100644
index 00000000000..244347e7ab5
--- /dev/null
+++ b/spec/models/custom_field_section_spec.rb
@@ -0,0 +1,37 @@
+# frozen_string_literal: true
+
+#-- copyright
+# OpenProject is an open source project management software.
+# Copyright (C) the OpenProject GmbH
+#
+# This program is free software; you can redistribute it and/or
+# modify it under the terms of the GNU General Public License version 3.
+#
+# OpenProject is a fork of ChiliProject, which is a fork of Redmine. The copyright follows:
+# Copyright (C) 2006-2013 Jean-Philippe Lang
+# Copyright (C) 2010-2013 the ChiliProject Team
+#
+# This program is free software; you can redistribute it and/or
+# modify it under the terms of the GNU General Public License
+# as published by the Free Software Foundation; either version 2
+# of the License, or (at your option) any later version.
+#
+# This program is distributed in the hope that it will be useful,
+# but WITHOUT ANY WARRANTY; without even the implied warranty of
+# MERCHANTABILITY or FITNESS FOR A PARTICULAR PURPOSE.  See the
+# GNU General Public License for more details.
+#
+# You should have received a copy of the GNU General Public License
+# along with this program; if not, write to the Free Software
+# Foundation, Inc., 51 Franklin Street, Fifth Floor, Boston, MA  02110-1301, USA.
+#
+# See COPYRIGHT and LICENSE files for more details.
+#++
+
+require "spec_helper"
+
+RSpec.describe CustomFieldSection do
+  it "uses the sidebar as default overview" do
+    expect(described_class.new).to be_shown_in_overview_sidebar
+  end
+end
diff --git a/spec/seeders/basic_data/project_custom_field_section_seeder_spec.rb b/spec/seeders/basic_data/project_custom_field_section_seeder_spec.rb
index da65a7931a3..6846f19a156 100644
--- a/spec/seeders/basic_data/project_custom_field_section_seeder_spec.rb
+++ b/spec/seeders/basic_data/project_custom_field_section_seeder_spec.rb
@@ -57,9 +57,9 @@ RSpec.describe BasicData::ProjectCustomFieldSectionSeeder do
     it "creates the corresponding sections with the given attributes", :aggregate_failures do
       expect(ProjectCustomFieldSection.count).to eq(2)
       expect(ProjectCustomFieldSection.find_by(name: "Project Attributes"))
-        .to have_attributes(position: 1)
+        .to have_attributes(position: 1, overview: CustomFieldSection::OVERVIEW__SIDEBAR_KEY)
       expect(ProjectCustomFieldSection.find_by(name: "Project Attributes Two"))
-        .to have_attributes(position: 2)
+        .to have_attributes(position: 2, overview: CustomFieldSection::OVERVIEW__SIDEBAR_KEY)
 
       # references the section in the seed data
       created_status = ProjectCustomFieldSection.last