The pretty conservation town of Ayton has had a long turbulent past. There is evidence of ancient human activity in the surrounding area including ring marks, stone circles, burial cairns and hill forts. The Romans are also known to have made incursions into the area.
Ayton Castle was originally a medieval tower house. The present castle dates largely from the 19th century and was designed by James Gillespie Graham and has been fully restored.
The nearby Ayton Old Church has been the scene of negotiations between King James IV and Henry VII of England. On 30 September 1497 they signed the treaty of Ayton whuch paved the way for a seven year truce.