The castle it once served was levelled around 1800, leaving this structure as the sole survivor of what was once a functioning medieval estate. Its corbelled roof, a technique in which stone courses are laid in overlapping rings until they close at the top, is left open at the apex, presumably to allow its original occupants to come and go freely. Those occupants were pigeons.

Dovecotes of this kind were serious pieces of agricultural infrastructure in medieval Ireland, and this one at Pottlerath is among the more complete examples to survive. The castle it accompanied was occupied in the 15th century, and the dovecote is considered likely to date from the same period. The building is roughly circular in plan, with an internal diameter of five metres and walls a metre thick. A round-headed doorway with cut limestone jambs opens into an interior where around 350 nesting niches line the walls from floor to nearly the full height of the structure. The floor sits slightly below the threshold of the doorway, a detail that presumably helped contain litter and nesting material. Pigeons kept in such a structure would have served two practical purposes for a medieval household: they were a reliable source of fresh meat, particularly useful in winter when other animals could not easily be slaughtered, and their accumulated droppings were collected as a highly valued fertiliser for kitchen gardens.

The dovecote sits approximately 140 metres to the east-north-east of where Pottlerath Castle once stood, in what is now open pasture. The castle itself has entirely disappeared above ground, which makes the dovecote's survival all the more arresting. The interior, with its rows of small rectangular niches covering every wall surface, gives a clear sense of the scale of pigeon-keeping that a moderately sized medieval estate might have maintained.