The place name itself carries an older strangeness: Ardfert derives from Ard Fhearta, most plausibly meaning the height of the burial mound. The building that rises from this ground is not one church but at least five, layered across roughly five centuries, and reading the fabric of its walls is something like reading a palimpsest where each generation left its corrections visible.

The early Christian foundation here is commonly attributed to St Brendan of Clonfert, whose fame as a sailor-monk has always attracted origin stories, but the evidence points more credibly to his tutor St Erc as the actual founder, sometime in the fifth century. The cathedral as it largely stands took shape around 1260, though it incorporated fragments of a twelfth-century Romanesque predecessor. That earlier work survives in the west wall: a round-arched doorway of two orders decorated with chevrons, trumpet capitals, and a barley-twist pillarette, with the lower sandstone blocks laid in a diamond pattern on either side. The thirteenth-century nave and chancel, measuring 44 by 8 metres, were built in uncoursed rubble limestone; the gables still stand to roughly ten metres, topped by crow-stepped battlements added in the fifteenth or sixteenth century. A south transept came in the fifteenth century, a vestry and mortuary chapel in the sixteenth, with further alterations recorded as late as 1668. The building's later history is one of damage and neglect: by 1584, in the aftermath of the Desmond rebellion, it was described in official correspondence as nearly prostrated and devastated. By 1611 it appeared on a parliamentary list of ruined cathedrals, with a proposal, apparently never acted upon, to transfer the cathedral see to Dingle. A widely repeated claim that it was destroyed in 1641 has been shown to lack foundation.

The cathedral was fully excavated over seven years by archaeologist Fionnbarr Moore, working alongside conservation works led by Grellan Rourke of the Office of Public Works. Human remains uncovered during the excavation were reinterred in the adjoining graveyard to the east. The site now operates as a managed visitor centre, and the conservation work means the architectural detail, the lancet windows with their cusped rear arches, the dog-tooth decoration on the chancel niches, the ogee-headed vestry door with its concave limestone jambs, can be examined at close range rather than glimpsed through scaffolding or overgrowth.