The old church appears to have been used as a place of worship until about the time of Charles I. The tradition is that the roof fell in on a Sunday after the congregation had left and were returning on the Brae of Powhillock to Auchterarder. While the old church continued to be the church of the parish, there was at an early period, and anterior to the Reformation, a chapel in the town of Auchterarder where the present parish church stands. The croft at the back is still named the Chapel Croft. The northern part of the present parish church and the steeple were erected about the middle of the seventeenth century, the steeple being built of stones taken from the old Castle of Kincardine, dismantled after the siege in 1646. The southern portion of the church was added in 1784.
There is incorporated with the parish of Auchterarder the eastern portion of the parish of Aberuthven. Aberuthven was one of the earliest ecclesiastical foundations in Scotland. It was dedicated to St. Cathan, Bishop and Confessor, who flourished in the sixth century. His festival was held on the 17th of May. The Churches of Kilchattan, in Bute, and Fortingall, in Perthshire, were also dedicated to him. Aberuthven was one of the churches appropriated to the Abbey of Inchaffray by the foundation charter of Gilbert, Earl of Strathearn, before referred to. The cure was served by a vicar appointed by that house. In the charter it is named "_Ecclesia Sancti Kattani de Abbyrrothueuen_." This charter was confirmed, and other churches granted by a subsequent charter of the Earl Gilbert. Alexander II. confirmed this last charter. Earl Malise confirmed by charter the gifts of his grandfather, Gilbert, and the confirmation of his father, Robert, Earl of Strathearn, and granted four merks of the rents of his lands of Aberuthven, which the Canons of Inchaffray were accustomed to receive previous to the year 1247.
Aberuthven continued a separate parish from Auchterarder until some time after the Reformation. It was united to Auchterarder prior to 21st February, 1618, and the minister for some time thereafter occupied the manse and glebe of Aberuthven. The parish of Aberuthven included the Brae of Foswell, south of the Ruthven, now partly situated in the parish of Auchterarder and partly in Blackford. Kincardine Castle, the seat of the Earls of Montrose, was within the bounds. Aberuthven was the parish church where that family worshipped and where their remains were interred. The walls of the Church of Aberuthven--a long, narrow building like that of Auchterarder--are still standing. On the south side, and partly within the area, a four-square building named "the Aisle" has been erected as a mausoleum for the ducal family of Montrose. The last received within its walls was James, Duke of Montrose, who died in 1836. This aisle was designed by Adam, the eminent architect. At the east end of the church, on the gospel side of the site of the high altar, there is a recess in the wall, forming an ambry of elegant form. It is evident there has been a door upon it, from the iron sockets which still remain. This was probably used for holding the church utensils. Worship was continued in Aberuthven Church until the end of the seventeenth century, as the funeral sermon of the Marchioness of Montrose was preached in it on 23rd January, 1673, by the Rev. Arthur Ross, the then parson of Glasgow, afterwards Archbishop of St. Andrews. His daughter, Anna, Lady Balmerino, was the mother of the gallant Lord Balmerino who was beheaded on Tower Hill in 1746.