The Church at Ayton dates back to the middle of the twelfth century. It was granted by the Scottish King Edgar to St Cuthbert’s Monks and thus became the property of the Priory of Coldingham of which it was a subordinate cell and remained such until the Reformation in 1560. It was dedicated to St Dionysius (St Denis – patron saint of France).

 In the year 1380 the Church was the scene on an important historical event – John of Gaunt along with the English commissioners, namely John, Bishop of Durham, Lord John Neville and John Waltham – the sub-Dean of York and representing Scotland, were John, Earl of Moray, Archibald Douglas, Lord of Galloway, James Douglas, Lord of Dalkeith and the Provost of St Andrews, Duncan Little met to arrange for a renewal of a truce between the two countries, and a similar meeting was held again in the Church in 1434. Then, on the 30th September 1497, a truce was entered into between Scotland and England that was to last seven years. It was signed in the Church of Ayton on behalf of King James IV of Scotland by his Ambassador, Andrew Forman.

The mediator of the last treaty was a Spanish clergyman Pedro d’Ayala who was, at that time, Ambassador to Ferdinand and Isabella of Spain at the court of King Henry VII of England. Also present, representing England, were the Bishop of Durham and William Wareham, master of the Rolls.

Probably the first Chaplain connected with this old Church in the present churchyard was Norman Parsona Cappellae de Ayton, the date of whose tenure of office is somewhat undefined, but was between the years 1166 and 1232.