diff --git a/app/controllers/application_controller.rb b/app/controllers/application_controller.rb
index 0b172c792b..f1f6027558 100644
--- a/app/controllers/application_controller.rb
+++ b/app/controllers/application_controller.rb
@@ -229,6 +229,16 @@ def current_ability
     end
   end
 
+  def handle_routing_error
+    if request.format == :json
+      render json: { errors: ["API action does not exist. Check that your URL and HTTP request method are correct."] }, status: :not_found
+    elsif request.format == :html
+      render file: Rails.root.join('public', '404.html').to_s, status: :not_found, layout: false
+    else
+      head :not_found
+    end
+  end
+
   def configure_permitted_parameters
     devise_parameter_sanitizer.permit(:sign_up) do |user_params|
       user_params.permit(:username, :email, :password, :password_confirmation)
diff --git a/config/routes.rb b/config/routes.rb
index 33b2b59afb..4c83b693e1 100644
--- a/config/routes.rb
+++ b/config/routes.rb
@@ -274,4 +274,11 @@
       end
     end
   end
+
+  # Routing errors are triggered in the middleware stack so can't be handled by
+  # a regular rescue_from block. Constraint is necessary to not break retrieval
+  # of things from active storage.
+  match '*unmatched', to: 'application#handle_routing_error', via: :all, constraints: lambda { |req|
+    req.path.exclude? 'rails/active_storage'
+  }
 end
diff --git a/spec/controllers/admin_collections_controller_spec.rb b/spec/controllers/admin_collections_controller_spec.rb
index 0ac38ebe0c..0c57ce0b53 100644
--- a/spec/controllers/admin_collections_controller_spec.rb
+++ b/spec/controllers/admin_collections_controller_spec.rb
@@ -417,13 +417,20 @@
         collection = Admin::Collection.find(JSON.parse(response.body)['id'])
         expect(collection.managers).to eq([])
       end
-      it "should return 422 if collection creation failed" do
+      it "should return 422 if unit not provided" do
         post 'create', params: { format:'json', admin_collection: { name: collection.name, description: collection.description } }
         expect(response.status).to eq(422)
         expect(JSON.parse(response.body)).to include('errors')
         expect(JSON.parse(response.body)["errors"].class).to eq Array
         expect(JSON.parse(response.body)["errors"].first.class).to eq String
       end
+      it "should return 422 if name not provided" do
+        post 'create', params: { format:'json', admin_collection: { description: collection.description, unit_id: collection.unit.id } }
+        expect(response.status).to eq(422)
+        expect(JSON.parse(response.body)).to include('errors')
+        expect(JSON.parse(response.body)["errors"].class).to eq Array
+        expect(JSON.parse(response.body)["errors"].first.class).to eq String
+      end
     end
 
     context 'when user does not have permissions for unit' do
diff --git a/spec/controllers/admin_units_controller_spec.rb b/spec/controllers/admin_units_controller_spec.rb
index 3821716d58..7e473941af 100644
--- a/spec/controllers/admin_units_controller_spec.rb
+++ b/spec/controllers/admin_units_controller_spec.rb
@@ -332,7 +332,7 @@
       unit = Admin::Unit.find(JSON.parse(response.body)['id'])
       expect(unit.unit_admins).to eq([administrator.username])
     end
-    it "should return 422 if unit creation failed" do
+    it "should return 422 if name not provided" do
       post 'create', params: { format: 'json', admin_unit: { description: unit.description } }
       expect(response.status).to eq(422)
       expect(JSON.parse(response.body)).to include('errors')
diff --git a/spec/controllers/media_objects_controller_spec.rb b/spec/controllers/media_objects_controller_spec.rb
index fd8b321883..48afc0182f 100644
--- a/spec/controllers/media_objects_controller_spec.rb
+++ b/spec/controllers/media_objects_controller_spec.rb
@@ -302,6 +302,17 @@
           expect(JSON.parse(response.body)["errors"].class).to eq Array
           expect(JSON.parse(response.body)["errors"].first.class).to eq String
         end
+        it "should return 422 if required fields are missing" do
+          media_object = FactoryBot.create(:published_media_object)
+          fields = {}
+          descMetadata_fields.each { |f| fields[f] = media_object.send(f) }
+          fields[:title] = nil
+          post 'create', params: { format: 'json', fields: fields, files: [master_file], collection_id: collection.id, publish: true }
+          expect(response.status).to eq(422)
+          expect(JSON.parse(response.body)).to include('errors')
+          expect(JSON.parse(response.body)["errors"].class).to eq Array
+          expect(JSON.parse(response.body)["errors"].first.class).to eq String
+        end
         it "should create a new media_object" do
           # master_file_obj = FactoryBot.create(:master_file, master_file.slice(:files))
           media_object = FactoryBot.create(:media_object)#, sections: [master_file_obj])
@@ -569,6 +580,17 @@
           expect(JSON.parse(response.body)["errors"].class).to eq Array
           expect(JSON.parse(response.body)["errors"].first.class).to eq String
         end
+        it "should return 422 if required fields are missing" do
+          media_object = FactoryBot.create(:published_media_object)
+          fields = {}
+          descMetadata_fields.each { |f| fields[f] = media_object.send(f) }
+          fields[:title] = nil
+          put 'json_update', params: { format: 'json', id: media_object.id, fields: { title: nil }, files: [master_file], collection_id: collection.id }
+          expect(response.status).to eq(422)
+          expect(JSON.parse(response.body)).to include('errors')
+          expect(JSON.parse(response.body)["errors"].class).to eq Array
+          expect(JSON.parse(response.body)["errors"].first.class).to eq String
+        end
 
         context "as an authorized non-admin user" do
           let(:user) { FactoryBot.create(:user) }
diff --git a/spec/requests/routing_error_spec.rb b/spec/requests/routing_error_spec.rb
new file mode 100644
index 0000000000..8c6ef00559
--- /dev/null
+++ b/spec/requests/routing_error_spec.rb
@@ -0,0 +1,35 @@
+# Copyright 2011-2026, The Trustees of Indiana University and Northwestern
+#   University.  Licensed under the Apache License, Version 2.0 (the "License");
+#   you may not use this file except in compliance with the License.
+#
+# You may obtain a copy of the License at
+#
+# http://www.apache.org/licenses/LICENSE-2.0
+#
+# Unless required by applicable law or agreed to in writing, software distributed
+#   under the License is distributed on an "AS IS" BASIS, WITHOUT WARRANTIES OR
+#   CONDITIONS OF ANY KIND, either express or implied. See the License for the
+#   specific language governing permissions and limitations under the License.
+# ---  END LICENSE_HEADER BLOCK  ---
+
+require 'rails_helper.rb'
+
+describe 'Routing Error Handling', type: :request do
+  it 'responds with 404 page for html request' do
+    get '/fake/route', params: { format: :html }
+    expect(response.status).to eq(404)
+    expect(response.body).to include('The page you were looking for doesn’t exist (404 Not found)')
+  end
+
+  it 'responds with json error for json request' do
+    get '/fake/route', params: { format: :json }
+    expect(response.status).to eq(404)
+    expect(JSON.parse(response.body)).to eq("errors" => ["API action does not exist. Check that your URL and HTTP request method are correct."])
+  end
+
+  it 'responds with 404 status for other request' do
+    get '/fake/route', params: { format: :atom }
+    expect(response.status).to eq(404)
+    expect(response.body).to be_empty
+  end
+end
diff --git a/spec/routing/media_objects_routing_spec.rb b/spec/routing/media_objects_routing_spec.rb
index 85e74773b2..d0e2d556f3 100644
--- a/spec/routing/media_objects_routing_spec.rb
+++ b/spec/routing/media_objects_routing_spec.rb
@@ -19,5 +19,8 @@
     it "routes to #move_preview.json" do
       expect(:get => "/media_objects/abc1234/move_preview.json").to route_to("media_objects#move_preview", id: 'abc1234', format: 'json')
     end
+    it "handles routing errors" do
+      expect(post: "/media_objects/abc1234").to route_to("application#handle_routing_error", unmatched: "media_objects/abc1234")
+    end
   end
 end