The east tower conforms to the usual layout of a Scottish tower house of the period, even though the building had earlier origins, as a gatehouse. The service buildings were on the ground floor, with the hall on the first floor and the private apartments on the two top floors. The great treasure of Huntingtower is the very rare painted ceiling in the first floor hall. It has been dated to c.1540 and that makes it a remarkable, almost unique survival. The ceiling panels are ornamented with a knotwork pattern in black on a white background. The patterns on the joists are painted in black and white on a red ground. The beams are decorated with leaves, scrolls and animal patterns. The walls also have traces of painted plaster indicating what a magnificent appearance this room must once have had.
The west tower is larger and a storey higher than its neighbour. Although the floorboards are no longer there, the traces of lozenge patterned wall decoration above the north door in the hall give an idea of how wonderful this room must have looked in the 16th century.
In 1487 James III created a later William Ruthven, Lord Ruthven. Patrick, the 3rd Lord Ruthven was one of the staunchest supporters of the Protestant Reformation in Scotland. He was a friend of Lord Darnley, Mary, Queen of Scots second husband and in September 1565 entertained the couple during their honeymoon. Lord Ruthven was one of those who participated in the murder of David Rizzio in 1566 and afterwards fled abroad, to Newcastle where he died soon after. His son, the 4th Lord Ruthven returned to Scotland in time to assist in the forced abdication of the Queen at Lochleven on 24 July 1567. He was present at the coronation of the queen's son, James VI at Stirling and was appointed treasurer of Scotland. In 1581 he was created earl of Gowrie.
Huntingtower or Ruthven Castle as it was called was the setting for the celebrated Scottish coup d'edat known as the 'Ruthven Raid'. In August 1582 Lord Gowrie and others anxious to remove the young king from Catholic influence took advantage of his presence in Perth to invite him to stay at Ruthven. The king accepted. He was held capture at Ruthven (Huntingtower) until June 1583 when the sixteen year old King managed to escape. James took his revenge and Lord Gowrie was tried, found guilty, and executed at Strirling in 1584. His property including Ruthven was forfeited to the crown, however James restored the estates and titles of the 1st Earl to his son James Ruthven. He died two years later and was succeeded by his younger brother John. John, the 3rd Earl Gowrie was also implicated in a conspiracy against James VI as a result of which the name of Ruthven was abolished, their arms deleted and all their lands forfeit. In 1600 Parliament also decreed that the place of Ruthven henceforth be called Huntingtower.
Huntingtower became crown property until in 1663 Charles II granted it to James Murray, earl of Tullabardine. When the 4th Earl of Tullabardine died at Huntingtower in 1670 without heir the property passed to his cousin, John Murray, 2nd Earl of Atholl, whose seat was Blair Castle. It was at Huntingtower that the 1st Duke of Atholl's wife gave birth to Lord George Murray, Bonnie Prince Charlie's military commander during the Jacobite Rebellion of 1745. In 1805 the 3rd Duke of Atholl sold Huntungtower to a local mill owner who used it to house his workers. Huntingtower was entrusted into the care of the state in 1912.