In the late 14th century John de Crichton (d.1406) built a tower house here as his family residence.
 John's son, William (d. c. 1453), served as Lord Chancellor of Scotland, and was made Lord Crichton in c. 1443.
In 1440 he had been partly responsible for organising the "Black Dinner", where the young William Douglas, 6th Earl of Douglas, was murdered.
As a result, he obtained the Douglas property of Bothwell Castle in Lanarkshire for himself.
John of Corstorphine, chief of Clan Forrester and a Douglas adherent, stormed and slighted the castle in 1445 in retaliation.
William, however, reconstructed and extended the castle, and also built the nearby collegiate church.
The 3rd Lord Crichton was a supporter of Alexander Stewart, Duke of Albany, and his lands and titles were forfeit in 1483, when Albany was sentenced for treason.
Crichton Castle, along with Bothwell Castle, was briefly granted to Sir John Ramsey, who forfeited it in 1488.

That year, James IV granted Crichton to Patrick Hepburn, Lord Hailes, who was later made Earl of Bothwell.
His son Adam, the second Earl, died at the Battle of Flodden in 1513.
Adam was succeeded by his son Patrick, who intrigued with the English against the Scottish crown, but eventually made peace with the regent, Mary of Guise.
James Hepburn, 4th Earl of Bothwell, sided with Mary of Guise during the Scottish Reformation, and when he took English money sent to the Lords of the Congregation, Regent Arran ordered an assault on Borthwick and Crichton, and the castle was besieged and captured by the Earl of Arran on 3 November 1560.

The castle was the scene of the marriage and wedding festivities, on 4 January 1562, of Patrick's daughter Jean (d. before July 1599) and John Stewart, Prior of Coldingham and illegitimate son of King James V. John Stewart's half-sister Mary, Queen of Scots, spent a few nights at the castle while attending this wedding.
The Earl of Bothwell was implicated in February 1567 in the murder of Queen Mary's husband Henry Stuart, Lord Darnley, and became Mary's third husband in May of that year.
In December, all Bothwell's titles and estates, including Crichton, were forfeited.

In 1568, Crichton, along with Bothwell's other estates, was granted to Francis Stewart, son of John Stewart and Jean Hepburn, and thus bastard grandson of James V. Francis was created Earl of Bothwell in 1577 and married Margaret Douglas.
He travelled in Europe, and he designed the very modern Italianate north range in the 1580s.
James VI was at Crichton on 17 March 1587, planning an embassy to Denmark with Peter Young.
Bothwell lost the king's favour and was accused of witchcraft and forfeited his estates in 1592.
He was eventually forced to flee to Naples where he died.
His son Francis Stewart was reinstated, but laboured under his father's debts, and sold Crichton to the Hepburns of Humbie.

J. M. W. Turner painted the castle, and it features in Sir Walter Scott's Marmion.
In 1956, the castle was given into state care by its owner, Major Henry Callander of Preston Hall.
It is now in the care of Historic Environment Scotland, and has been a scheduled monument since 1921.
Crichton was used as a location in the 1995 film Rob Roy and the 2011 film The Wicker Tree.
In the late 14th century John de Crichton (d.1406) built a tower house here as his family residence.  John's son, William (d. c. 1453), served as Lord Chancellor of Scotland, and was made Lord Crichton in c. 1443. In 1440 he had been partly responsible for organising the "Black Dinner", where the young William Douglas, 6th Earl of Douglas, was murdered. As a result, he obtained the Douglas property of Bothwell Castle in Lanarkshire for himself. John of Corstorphine, chief of Clan Forrester and a Douglas adherent, stormed and slighted the castle in 1445 in retaliation. William, however, reconstructed and extended the castle, and also built the nearby collegiate church. The 3rd Lord Crichton was a supporter of Alexander Stewart, Duke of Albany, and his lands and titles were forfeit in 1483, when Albany was sentenced for treason. Crichton Castle, along with Bothwell Castle, was briefly granted to Sir John Ramsey, who forfeited it in 1488.
That year, James IV granted Crichton to Patrick Hepburn, Lord Hailes, who was later made Earl of Bothwell. His son Adam, the second Earl, died at the Battle of Flodden in 1513. Adam was succeeded by his son Patrick, who intrigued with the English against the Scottish crown, but eventually made peace with the regent, Mary of Guise. James Hepburn, 4th Earl of Bothwell, sided with Mary of Guise during the Scottish Reformation, and when he took English money sent to the Lords of the Congregation, Regent Arran ordered an assault on Borthwick and Crichton, and the castle was besieged and captured by the Earl of Arran on 3 November 1560.
The castle was the scene of the marriage and wedding festivities, on 4 January 1562, of Patrick's daughter Jean (d. before July 1599) and John Stewart, Prior of Coldingham and illegitimate son of King James V. John Stewart's half-sister Mary, Queen of Scots, spent a few nights at the castle while attending this wedding. The Earl of Bothwell was implicated in February 1567 in the murder of Queen Mary's husband Henry Stuart, Lord Darnley, and became Mary's third husband in May of that year. In December, all Bothwell's titles and estates, including Crichton, were forfeited. 
In 1568, Crichton, along with Bothwell's other estates, was granted to Francis Stewart, son of John Stewart and Jean Hepburn, and thus bastard grandson of James V. Francis was created Earl of Bothwell in 1577 and married Margaret Douglas. He travelled in Europe, and he designed the very modern Italianate north range in the 1580s. James VI was at Crichton on 17 March 1587, planning an embassy to Denmark with Peter Young. Bothwell lost the king's favour and was accused of witchcraft and forfeited his estates in 1592. He was eventually forced to flee to Naples where he died. His son Francis Stewart was reinstated, but laboured under his father's debts, and sold Crichton to the Hepburns of Humbie. 
J. M. W. Turner painted the castle, and it features in Sir Walter Scott's Marmion. In 1956, the castle was given into state care by its owner, Major Henry Callander of Preston Hall. It is now in the care of Historic Environment Scotland, and has been a scheduled monument since 1921. Crichton was used as a location in the 1995 film Rob Roy and the 2011 film The Wicker Tree.
Crichton Castle