Huntingtower Castle was built in the early 15th century by the Ruthven family, and was then known as the Place of Ruthven or Ruthven Castle.

Ruthven Castle was the location of the Raid of Ruthven, when on the 22nd of August 1582 several Presbyterian nobles, led by William Ruthven the 4th Lord Ruthven and 1st Earl of Gowrie, imprisoned King James VI in the castle and held him for 10 months.

Following a second plot against the king in 1600 known as the Gowrie Conspiracy, this time carried out by John and Alexander Ruthven, two of of William Ruthven's sons, James executed the ringleaders, seized the estates and proscribed the name of Ruthven. It was at this time that the castle became known as Huntingtower. The castle was kept by the Crown until 1643 when it passed to the family of Murray of Tullibardine.

Originally it was a three storey tower (the part now forming the east part of the building, and known as the "Eastern Tower"), but towards the end of the 15th century a second L-shaped tower (the "Western Tower") was built just 3 metres away from it, joined by a wooden bridge just below the battlements. It is said this was to separately accommodate the households of two brothers, John and Alexander, the sons of William Ruthven, but they lived a century too late for the story to be true.

There were ancillary buildings around the castle, and the whole property was surrounded by a defensive wall. In the late 16th century a great hall was built on the north side of the Western Tower, and although it has now been removed, the remains of its pitched roof can still be seen on the castle wall, with slates protruding.

The Murrays built up the space between the two towers in the 17th century, making the castle as it appears today. The Murray family remained in the castle until 1767 when John Murraythe 1st Duke of Atholl's wife died, and he moved out. It was used for a while by farm labourers but fell into disrepair, and passed into state care in 1912.

Huntingtower Castle is remarkable for the early 16th century wooden ceiling on the first floor of the Eastern Tower, which are painted with designs including animals, dragons and knotwork. On the walls of the same room are the remains of painted plasterwork from the same period, and these feature a hare, an angel, a deer and flowers.