The first church was founded by Constantin, King of the Picts, about 800 A.D., and the Culdees were established in a monastery here. In 1107 it became the seat of a bishopric, and a colony of Augustinian canons replaced the former dwellers. A new choir was built in 1220-1250, in the Early English style. During the wars with England, in 1380, it was burnt, but almost immediately restored. The nave was finished by Bishop Lauder in 1465. He was a most munificent prelate, who did much for his Cathedral, began the tower and chapter-house, and furnished the Cathedral with gifts of much valuable church plate. There is a curious story[21] of a Highlanders' raid, and of their entry to the church, and of the bishop's perilous escape to the rafters of his church, in order to escape their hands. On another occasion the church was besieged in the time of the famous Bishop Gavin Douglas, the translator of the Æneid (1576). His election to the see was opposed by the Stewarts, the inveterate enemies of his house; and Andrew Stewart barred the door against him, and fought against him from his stronghold in the tower. Douglas soon gathered his friendly clans together, and forced an entrance. It is uncertain when the nave lost its roof, probably when certain lairds at the Reformation went on their base crusade, plundering and destroying churches, and seizing their goods and valuables.

After the battle of Killiecrankie there was a great fight here, and an asylum of refuge was found here by the people, who fortified their position with the seats, and did much damage. The roof was destroyed, and the nave has been ever since exposed to the storms of wind and rain. The choir is now used as the parish church, having been rebuilt. The nave has seven bays, and measures 120 feet by 60 feet. The piers are of massive Norman character, and there is a somewhat poor triforium and clerestory. The original choir was built by Bishop Sinclair in 1350. The tower, 96 feet high, is Perpendicular, the work of Bishop Lauder (1469), and finished by Bishop Brown in 1501, and is a very good example of the style. The south porch was built by Lauder, but it is now in ruins. The chapter-house is the work of the same bishop. It contains the vault of the Dukes of Athol. Here, near the porch, is buried Alexander Stuart, Earl of Buchan, better known as the "Wolf of Badenoch" (1394), who burned down Elgin Cathedral and devastated the place. Few churches have passed through such stormy scenes as Dunkeld, and its ruined state is a melancholy testimony to the lawlessness of the tumultuous times, which have left their mark upon its desecrated walls.