This double-towered castle started life as the Place (or House) of Ruthven during the 15th century. It was built by Clan Ruthven in stages with two tower houses separated by a gap of less than 10 feet (three metres).
Mary Queen of Scots honeymooned here with Lord Darnley in 1565. However, the Earl of Gowrie of Clan Ruthven fell out of favour with James VI of Scotland. The earl was executed in 1600 and the Place of Ruthven siezed in the name of the Crown and renamed Huntingtower Castle. In 1643 it was given to the family of Murray of Tullibardine, from whom the Dukes of Atholl of Blair Castle [cross-ref] are descended.
The Murrays built in the narrow gap between the towers later in the 17th century, creating the castle we see today. Other nearby buildings, including a great hall, were enclosed by a defensive stone wall, but almost nothing of them survives. It stopped being a grand residence about a century later, and was abandoned in 1767.
In the east tower is one of the oldest painted ceilings in Scotland and some fragments of wall paintings. The property is in the care of Historic Scotland.