The land had been set aside in the reign of Alexander I of Scotland, in an area known as the Cursus Apri, the Boar's Run, where legend claimed an enormous boar had once been killed. David I and his son completed the foundation in 1140. The Augustinians took the main altar of the cathedral. The Culdees, headed by their own abbot, kept a side altar and the older buildings nearby. A papal bull of 1147 ordered that each time a Culdee died, an Augustinian should take his place, gradually absorbing the older order. The Culdees outlasted that schedule. They were still there in 1199, when the new priory formally recognized their holdings as permanent. Only by 1250 did those who refused to convert finally move out to the small Church of St Mary on the Rock at Kilrymont, where they survived another two centuries as a Collegiate Church in the cathedral's shadow.

The canons managed the shrine of St Andrew, which made St Andrews one of the most important pilgrimage destinations in Western Europe. Legend, taught by every priest in town, said that the apostle Andrew's relics had been brought to Scotland by St Rule from Patras in Greece in the 4th century. The truth was probably mistier, involving a piece of bone donated by an earlier Anglo-Saxon monastery, but the pilgrim trade did not care about provenance and the canons did not undeceive them. The priory ran a hospital. It accumulated dependent houses across Fife and beyond: St Serf's Inch on Loch Leven, Monymusk in Aberdeenshire, the Isle of May, Pittenweem after the Isle of May community relocated there in 1318, Portmoak Chapel. In 1349 the Black Death came. Twenty-four canons died. The priory mourned, regrouped, and kept going.

Around Pentecost 1410, Prior James Biset opened a school of higher studies inside the priory walls. The teachers were Augustinian scholars who had been driven out of the University of Paris by the Avignon Schism and out of Oxford and Cambridge by the Anglo-Scottish Wars. They offered lectures in divinity, logic, philosophy, and law. Bishop Henry Wardlaw bestowed a charter of privilege on the society of masters and scholars. From that small school grew the University of St Andrews, Scotland's first university and the third-oldest in the English-speaking world. The university is the priory's most consequential descendant. It still exists. The priory does not.

On a June day in 1559, with the Scottish Reformation arriving at full speed, a mob inflamed by the preaching of John Knox ransacked the cathedral and the priory. The interiors were destroyed. The community of canons, already shrunken and demoralized by decades of lay commendators skimming the income, ceased to function. The priory lands were carved up into lordships in the 16th century, though the title lingered into the 17th. The east and south ranges of the medieval priory buildings survive as fragments around the modern St Andrews Cathedral Museum. The Pends, a 14th-century stone gatehouse that once welcomed pilgrims and merchants from across Europe, still stands at the entrance to the cathedral grounds. A piece of the guest-house wall remains. The land that once belonged to the priory now includes the grounds of Rufflets Hotel between Strathkinness and St Andrews. The priory is gone. Its university outlived it. So did the question of whether you can ever really replace one religious culture with another, or whether they only ever layer over each other, like the stones of the wall that the canons and the Culdees once shared.