St Caillín, said to have descended from the Conmaicne Cúile Tolad around Dunmore in Co. Galway, supposedly received the site as a gift from Aodh Finn, son of Feargna of the Uí Briuin Breifne, after that druidic transformation, and went on to accumulate a notable collection of relics during a visit to Rome. The principal source for his life is the Book of Fenagh, held by the Royal Irish Academy, which was copied in 1516 from an earlier manuscript written around 1350 to 1400. That earlier book is now missing, though it may once have been kept inside St Caillín's book shrine, a decorative reliquary container made to protect a venerated manuscript. That shrine, along with the shrine of St Caillín's Bell, was stored at St Mel's Cathedral in Longford, where both were damaged in a fire on Christmas Day 2009. Scholars have treated the hagiographical details with some scepticism, but the site itself accumulated a well-documented institutional history regardless of what can be verified about its founder.

The place-name Fenagh derives from the Irish Fidnach or Fiodhnach, meaning wooded, and the church here became the principal ecclesiastical centre associated with the O'Rourkes, though that family never appears to have exerted direct control over it. The site maintained its own Rule into the later Middle Ages, operating with a degree of independence unusual for a church so closely tied to a regional lordly family. By 1125, when a Viking raid on the termon, the protected lands surrounding the church, was recorded as having been foiled, the settlement was clearly of some importance. The coarbs, a term for hereditary ecclesiastical successors who administered such sites and were generally drawn from the O'Rodachain or Roddy family, are first mentioned in 1244, at which point the church was already described as roofless. The church was accidentally burnt in 1360, and the structure standing today may date from after that fire. In 1585 its nine quarters of land were transferred to the Protestant bishop of Ardagh, though the O'Rodaighe family, regarded as accomplished scholars, remained in the area until at least 1706. The Down Survey maps of 1656 to 1658 show both churches on the site already roofless, and the principal church may later have been put to Protestant use before the nearby Church of Ireland church of St Catherine was built around 1800.

The surviving church is a complete, if roofless, structure roughly 26 metres long and 7 metres wide, with dressed quoins and a barrel vault at the western end that likely supported a defensive residential tower above. The eastern window retains fine 15th-century tracery, four cusped ogee-headed lights beneath a rosette, with three carved stone heads along its hood moulding. Face-corbels appear at each corner of the building, and a carved rabbit decorates a string-course on the north wall. Inside, a piscina and a double sedilia, a shallow basin for rinsing chalices and a pair of recessed seats for clergy, occupy the south wall near the east end. Abutting the south wall is a small roofless chapel or mausoleum belonging to the O'Duignans of Castlefore, with a Latin commemorative plaque dated 1671 on its exterior. The whole complex sits within a roughly circular earthwork enclosure about 110 metres in diameter, itself embedded in a much larger system of grass-covered banks and field boundaries covering around 15 hectares. These earthworks, which are most legible from the air, are likely early medieval in origin and sit beneath and around the later rectangular graveyard, where headstones date from around 1760 to the present.