In the late 14th century John de Crichton built a tower house here as his family seat - a stone keep on a rise above the head of the River Tyne, two miles south of the modern village of Pathhead. His son William served as Lord Chancellor of Scotland and was made Lord Crichton around 1443. Three years earlier, in 1440, William had been one of the organisers of the Black Dinner: the young William Douglas, 6th Earl of Douglas, was invited as a guest to Edinburgh Castle and murdered with his brother in front of the 10-year-old King James II. The killing broke the power of the House of Douglas. As a reward, Crichton obtained the Douglas property of Bothwell Castle in Lanarkshire for himself. John of Corstorphine, chief of Clan Forrester and a Douglas adherent, stormed Crichton in 1445 in retaliation and slighted - partly destroyed - the castle. William rebuilt it on a grander scale, adding a second tower to form an L-plan, and also built the nearby Crichton collegiate church.

In 1483 the 3rd Lord Crichton lost the castle when his patron Alexander Stewart, Duke of Albany, was sentenced for treason. Five years later King James IV granted it to Patrick Hepburn, Lord Hailes - the man who would soon be made the 1st Earl of Bothwell. The Hepburns of Bothwell were one of the most powerful families in Scotland, and Crichton became their seat. Patrick's son Adam, the 2nd Earl, died at the Battle of Flodden in 1513 alongside the king and most of the Scottish nobility. The castle passed to Adam's widow, Lady Agnes Stewart, who promptly married Alexander Home, 3rd Lord Home, in 1514. Their son Patrick Hepburn, 3rd Earl of Bothwell, inherited Crichton in time to participate in the destabilisation of Scotland during the minority of Mary, Queen of Scots - intriguing with the English, then making peace with the Regent Mary of Guise.

On 4 January 1562, Crichton hosted the wedding of Patrick Hepburn's daughter Jean to John Stewart, Prior of Coldingham and illegitimate son of King James V. The bride's new sister-in-law - John Stewart's half-sister Mary, Queen of Scots herself - attended the wedding and spent several nights at the castle. Five years later, in 1567, James Hepburn, 4th Earl of Bothwell - Jean's brother and Mary's bridegroom-to-be - was implicated in the February murder of Mary's husband Lord Darnley. In May, Mary married Bothwell. By December all Bothwell's titles and estates were forfeited. Crichton passed to Francis Stewart, the bastard grandson of James V through John Stewart and Jean Hepburn's marriage. Francis was created Earl of Bothwell in 1581. He travelled extensively in Europe, and in the 1580s he came home with a head full of Renaissance ideas.

Francis Stewart designed the Italianate north range himself. The courtyard façade was modelled on the Palazzo dei Diamanti, the Diamond Palace built in Ferrara in the 1490s - one of the most distinctive buildings of Italian Renaissance architecture, faced with thousands of pointed diamond-cut stones. Francis brought the technique back to Midlothian and applied it to a small section of Crichton's courtyard. Inside the range he installed innovations: Scotland's first 'scale-and-platt' staircase, a modern stair with broad landings between flights, and a proper drawing room - rooms specifically for sitting and talking, not just for sleeping or eating. His initials and his wife Margaret Douglas's appear on the walls, together with a carved anchor representing his position as Lord High Admiral of Scotland. King James VI visited him here on 17 March 1587 to plan an embassy to Denmark.

Francis Stewart lost the king's favour in the early 1590s. He was accused of witchcraft - the North Berwick trials of 1590-92 had created an atmosphere in which any nobleman the king distrusted could be linked to occult conspiracy - and forfeited his estates in 1592. He fled Scotland and eventually reached Naples, where he died. The castle passed to his son Francis Stewart, who tried to recover the family fortunes but failed under his father's debts and sold Crichton to the Hepburns of Humbie. The castle slowly decayed. J. M. W. Turner painted it in the early 19th century as a romantic ruin. Walter Scott included it in his 1808 poem Marmion. In 1956 it was given into state care by Major Henry Callander of Preston Hall, and has been scheduled as a national monument since 1921. It featured in the 1995 film Rob Roy and the 2011 film The Wicker Tree. The diamond wall is still there, still standing, still throwing its pyramid shadows across the courtyard, still the only one of its kind in Scotland.