It was on the pilgrim's route from St Andrews to Santiago de Compostela and described as a stopping point in the Iter pro peregrinis ad Compostellam., Book V of the Codex Calixtinus.

The shrine of Our Lady at Whitekirk was desecrated by the armies of Edward III of England in 1356, a period that would become known as the Burnt Candlemas.

Whitekirk continued to be a place of pilgrimage, however, receiving visits from the future Pope Pius II and James IV, Margaret Tudor, and James V.[2] In early 1435 Aeneas Piccolomini (Pope Pius II) was travelling to Scotland on a diplomatic mission as Papal legate when his ship was beset by storms.

After giving prayers to Our Lady, the ship and its crew made port safely at Dunbar, and having promised to walk barefoot to the nearest shrine to the virgin, Piccolomini set out for Whitekirk.

From 1806 to 1852 the minister of Whitekirk was the Rev James Wallace, who served as Moderator of the General Assembly in 1831/32, the highest position in the Church of Scotland.