It housed the burgh’s wealthy and powerful bishops while St Andrews served as the ecclesiastical centre of Scotland during the years before the Protestant Reformation.

In their Latin charters, the Archbishops of St Andrews wrote of the castle as their palace, signing, "apud Palatium nostrum.

In 1314, however, after the Scottish victory at Bannockburn, the castle was retaken and repaired by Bishop William Lamberton, Guardian of Scotland, a loyal supporter of King Robert the Bruce.

Sir Andrew Moray, Regent of Scotland in the absence of David II, recaptured it after a siege lasting three weeks.

James I of Scotland (1406–1437) received part of his education from Bishop Henry Wardlaw, the founder of the University of St Andrews in 1410.

Beaton altered the defences to enable the castle to withstand a heavy artillery attack, which was a threat as tensions grew between English Protestants and Scottish Catholics.

Christopher Grymmerschere, a French military engineer, provided guns, and Master Wolf made new cannon, and John Fynnyk was the castle gunner.

Arran heard that an English army was on its way to relieve the Castle and asked Fife Lairds like John Wemyss of that Ilk to come by 4 November 1546, bringing his followers and whatever artillery they had to resist a sea invasion.

[6] Although Henry VIII made plans to assist the Protestants within the castle,[7] the invasion never came and his son Edward VI did not send aid.

This peaceful interlude came to end, however, when a French fleet arrived bringing an Italian engineer Leone Strozzi who directed a devastating artillery bombardment to dislodge the Protestant lairds.

The lairds knew an expert was in the field when their own Italian engineer observed cannon being winched into position with ropes rather than exposing the besiegers to their fire.

Following this Protestant defeat, the castle was substantially rebuilt by Archbishop John Hamilton, the illegitimate brother of Regent Arran, and successor to Dr. David Cardinal Beaton.

With the eventual success of the Reformation in Scotland, the office of the bishop was increasingly eroded until it was finally abolished by William of Orange in 1689.