The stones were taken down by Captain Nickson of Money and used to build a 3.6-metre-high enclosure wall across the western end of the church interior, converting a portion of an ancient place of worship into a private family burial plot. The south wall is now almost entirely gone as a result, and the Nixon family tomb still stands inside the building, a reminder that the ruin was not only shaped by time and neglect but by a fairly brazen act of appropriation. A 1944 National Monument Order eventually prohibited further burials within the designated area surrounding the church, closing a loop that had been open for rather too long.

The site itself has roots going back to the sixth century. The name Aghowle derives from the Irish Achadh-Abhall, meaning field of the apple trees, and the monastery here was founded by St. Finnian of Clonard, Co. Meath, with dates given in the sources as 549 to 592. The Annals of the Four Masters record the death of the Abbot of Aghowle in 1018, and the death of its erenagh, a hereditary church official responsible for managing ecclesiastical lands, in 1050. By 1204 the church was listed among the possessions of Herluin, Bishop of Leighlin, and a taxation record from 1302 to 1306 valued it at 40 shillings. In 1418 the pope appointed Thady Obryn to the canonry and prebend of Aghowle, filling a vacancy left by the resignation of one William Yaega. Public worship finally ceased here in 1716, when the congregation moved to St. Michael's Church of Ireland at Coolkenna, and by the time the Ordnance Survey recorded the site in 1838 to 1840, the area around it had long been described as formerly much encompassed with bogs and difficult of approach in winter.

What survives today is a Romanesque church, 18 metres long and just over 7 metres wide, built predominantly from granite field stones with some schist, its walls averaging 90 centimetres thick. Both gables and the north wall remain well-preserved. The west gable retains a finely made trabeate doorway, that is, one with a flat lintel rather than an arch, nearly 2 metres high and slightly narrowing from base to top, with roll moulding and a double architrave framing the exterior. A window sits in the apex of the same gable, and corbels suggest a former internal gallery. The east gable holds a pair of windows, an aumbry, and traces of a piscina, small recessed features used in liturgical practice for storing vessels and disposing of holy water. Scattered across the wider site are cross slabs, architectural fragments, fonts, and a granite bullaun stone, a boulder with a cup-shaped hollow used for grinding or ritual purposes, located around 100 metres to the south-east. St. Finnian's High Cross also stands here, its head reattached with stone pins during late nineteenth-century repairs.