Huntingtower Castle was built in stages from the 15th century and was known for several hundred years as the 'House of Ruthven'.

In 1582, the castle was occupied by the 4th Lord Ruthven, and 1st Earl of Gowrie who was involved in a plot to kidnap the young King James VI, son of Mary Queen of Scots. Gowrie and his associates seized the young king and held him prisoner for 10 months. James eventually escaped and actually forgave Gowrie, but after a second abortive attempt by Gowrie and others to overthrow him, Gowrie was executed and his property forfeited to the crown.

The Castle and lands were restored to the Ruthven family in 1586 however once again, in 1600, John and Alexander Ruthven were implicated in another plot to kill King James VI and were executed. As well as seizing the estates, the King abolished the name of Ruthven and decreed that any successors would be ineligible to hold titles or lands. Thus the House of Ruthven ceased to exist and by royal proclamation the castle was renamed Huntingtower.

The Castle remained in the possession of the crown until 1643 when it was given to the family of Murray of Tullibardine. John Murray, 1st Duke of Atholl, resided in the Castle until the death of his wife in 1767 and the castle was abandoned.