diff --git a/wagtail/wagtailadmin/templates/wagtailadmin/shared/field.html b/wagtail/wagtailadmin/templates/wagtailadmin/shared/field.html
index 7cb6c05c7..0a87112ad 100644
--- a/wagtail/wagtailadmin/templates/wagtailadmin/shared/field.html
+++ b/wagtail/wagtailadmin/templates/wagtailadmin/shared/field.html
@@ -4,7 +4,7 @@
     <div class="field-content">
         <div class="input {{ input_classes }} ">
             {% block form_field %}
-                {{ field }}
+                {{ field|render_with_errors }}
             {% endblock %}
             
             {# This span only used on rare occasions by certain types of input #}
@@ -14,7 +14,7 @@
             <p class="help">{{ field.help_text }}</p>
         {% endif %}
 
-        {% if field.errors %}
+        {% if field|has_unrendered_errors %}
             <p class="error-message">
                 {% for error in field.errors %}
                     <span>{{ error|escape }}</span>
diff --git a/wagtail/wagtailadmin/templatetags/wagtailadmin_tags.py b/wagtail/wagtailadmin/templatetags/wagtailadmin_tags.py
index 650e49f35..993b83ecc 100644
--- a/wagtail/wagtailadmin/templatetags/wagtailadmin_tags.py
+++ b/wagtail/wagtailadmin/templatetags/wagtailadmin_tags.py
@@ -150,3 +150,27 @@ class EscapeScriptNode(template.Node):
         return cls(nodelist)
 
 register.tag(EscapeScriptNode.TAG_NAME, EscapeScriptNode.handle)
+
+
+# Helpers for Widget.render_with_errors, our extension to the Django widget API that allows widgets to
+# take on the responsibility of rendering their own error messages
+@register.filter
+def render_with_errors(bound_field):
+    """
+    Usage: {{ field|render_with_errors }} as opposed to {{ field }}.
+    If the field (a BoundField instance) has errors on it, and the associated widget implements
+    a render_with_errors method, call that; otherwise, call the regular widget rendering mechanism.
+    """
+    widget = bound_field.field.widget
+    if bound_field.errors and hasattr(widget, 'render_with_errors'):
+        return widget.render_with_errors(bound_field.html_name, bound_field.value(), attrs={'id': bound_field.auto_id}, errors=bound_field.errors)
+    else:
+        return bound_field.as_widget()
+
+@register.filter
+def has_unrendered_errors(bound_field):
+    """
+    Return true if this field has errors that were not accounted for by render_with_errors, because
+    the widget does not support the render_with_errors method
+    """
+    return bound_field.errors and not hasattr(bound_field.field.widget, 'render_with_errors')