According to local tradition, St. Feidhlimidh founded a small church on the site in the 6th century.

In 1455 the old Catholic Parish Church of St. Feidhlimidh became the cathedral for the Kilmore Diocese, continuing after the Reformation as Kilmore Church of Ireland Cathedral, even after the Kilmore See was amalgamated in 1841 with those of Elphin and Ardagh.  However, by 1858 the building was too small and dilapidated and the present cathedral, designed by William Slater, was built by 1860 alongside the old one, which is now used as a parochial hall.

The historic 1860 organ, one of the earliest organs built by Charles Brindley of Sheffield was restored in 2011