In the 14th century John de Crichton built a tower house on the site. His son William served as Lord Chancellor of Scotland and was created Lord Crichton in c.1443. He had been partly responsible for organizing the infamous 'Black Dinner' of 1440 when the young Earl of Douglas was murdered. As a consequence he obtained the Douglas property of Bothwell Castle in Lanarkshire. In retaliation a Douglas loyalist attacked Crichton in 1445. William not only made good the damage but extended the castle and built the nearby collegiate church. But the 3rd Lord Crichton Castle made the mistake of supporting the Duke of Albany and as a result, lost his land and titles which were forfeit in 1483.
In 1488 James IV granted Crichton Castle to James Hepburn, later 1st Earl of Bothwell. The 2nd Earl died at Flodden in 1513. The 3rd Earl conspired with the English against the Scottish Crown but eventually made his peace with the regent Mary of Guise. When the 4th Earl of Bothwell sided with the Catholic Mary of Guise during the Scottish Reformation, Regent the Earl of Arran attacked and captured Crichton on 3rd November 1560.
Crichton Castle was the venue for a glittering social occasion on 4th January 1562, the marriage of Jean Hepburn to John Stuart, Lord Darnley, illegitimate son of James V, whose half sister Mary Queen of Scots attended the festivities.
The Earl of Bothwell was implicated in the murder of Mary's second husband Henry Stuart, Lord Darnley, in February 1567, and became Mary's third husband in May of that year. By December all Bothwell's estates, including Crichton and his titles, were forfeited.
In 1568 Bothwell's estates, including Crichton, were granted to Francis Stewart, son of John Stewart Lord Darnley, and Jean Hepburn, therefore grandson of James V. Francis was created Earl Bothwell in 1577. He was a highly cultured and educated man who traveled widely in Europe, and inspired by what he had seen built the ultra-modern Italianate North range at Crichton in the 1580's.
Francis Stewart entertained James VI at his astonishing new lodging in March 1586. The king himself a cultured man must have been suitably impressed. But the Earl's volatile and impetuous nature propelled him into exile in 1595 and he never returned to Scotland. We are incredibly lucky that the King's order to raise the castle was never carried out. But Crichton ceased to be a lordly residence. Although the castle was restored to his son, also Francis, he was shackled by debt and sold up. By 1659 the stones of Crichton were being carried away for use in other buildings.
In Marmion, Sir Walter Scott described the neglected ruins:
Crichton! though now they miry court
But pens the lazy steer and sheep
But interest in the ruins generated by the publication of Marmion led to Crichton being valued again and in 1926 the still splendid ruined castle was handed over to the care of the State.