Huntingtower is a charmingly curious castle. The structure consists of two separate tower houses, of a type common from the north of England through the Borders up into Scotland, which were subsequently joined together to form a larger residence. The arrangement of rooms inside very much reflects this unusual history, which tells its own story of the needs of its former owners.

The site, outside the town of Perth, is naturally protected on the west by a narrow valley, and on the north by a steep bank descending to the river. The east and south sides are open and unprotected; no evidence suggests defensive banks or ditches, but there were probably formal gardens and orchards here during its occupation.

The eastern tower is the earlier, with the fifteenth century gatehouse having been enlarged to form the three storeys and a garret in around 1500. The original arched entrance to the passageway into the courtyard is still visible, as is the spring of the vault on the inside. A mezzanine wooden floor was constructed, but then replaced by the existing stone barrel vault. On the first floor was the solar, or main residential hall. The fireplace is from a later remodelling, otherwise this room looks much as it must have during the early part of the sixteenth century. On the north side is a rectangular window, with seats, and to the left of the fireplace, where a cupboard originally was, another window now helps to provide light. The stunning painted wooden ceiling of this room, dating from around 1540, was only revealed by the removal of later pine panelling in 1913. Although sore on the neck, it is well worth spending some time examining the various designs, from knotwork, to botanical to zoomorphic. The remaining traces of painted plaster in the room seem to date from even earlier; again, time to trace out the features is well rewarded. The second floor room has a fine early sixteenth century fireplace, useful cupboards and shelves, again, seats at the window, and a private latrine. The garret was reached by a door in the west gable.

Around the same time as the eastern tower was being remodelled, the western tower was constructed about 3m away. The extraordinarily small distance between the towers is presumed to be a result of the division of the land between two brothers, William, the Master of Ruthven, and John. It seems that each tower was used as a separate residence for their respective families, but the proximity would provide extra security and shared use of out buildings. The Western tower is slightly larger than the East, with a projecting chamber-block rising to four storeys. Again, the first floor would have been the hall, but the floors in this tower have not survived, and the features are mostly those of the seventeenth century rebuilding, when the connecting walls between the two towers was built. However, some wall paintings from the original rooms survive – the remains of a coat of arms, datable to pre-1513, as John Erskine of Dun, whose arms appear on the right hand side, was killed at the battle of Flodden in that year, and his wife, Margaret of Ruthven, had remarried by 1518. The garret on top of the West tower housed a dovecot, to provide fresh meat for the families.