The church and its cemetery were founded in 1652-1656, when Oliver Cromwell took over the older church of St John as part of his Fort or Citadel. Because he had used their older church as a place to store weapons, Cromwell ordered his Major General Deane to give 1000 merks to the people of Ayr towards the cost of building a new church.

But the site chosen for the new church was not unconnected with religion. The Grey Friars, or Franciscans, had arrived in Ayr by invitation in 1474, and in 1481 the Pope agreed to their building a friary. The site of the Friars' Well is shown on old maps of the town, this was located in the Kirkyard.

Dating from 1656 is the large covered lychgate which guards the entrance to the churchyard from the Kirk Port.

Lychgates are more common in England and are rare in Scotland. It's possible that this one has its origins in Cromwell's connection with the building of the church.

It was the law to go to church in those days and if you didn't go you got fined. People went to church all day. They came in the morning and had a service then they had lunch under the lychgate if it was raining.

The rich sat up in the lofts to eat their lunch with their servants, and had fires to keep warm.

During the week, the covered lychgate was used during funerals. Coffins were kept there while waiting for the minister to come to start the funeral service.

At one time there were grave robbers who tried to steal bodies for doctors and hospitals to use in research. To stop them stealing bodies from the Auld Kirk, there were heavy cast-iron frames called Mort Safes which were put on the coffins after the funeral, and buried with them, to stop anyone lifting the lid to take out a body. Once the body had decayed the mort-safe was removed and used on another coffin.