The first church in Derrylin was built in 1797. The inscription on the date stone reads “Haec est Domus Dei et porta coeli, fundamentum me fecit Michaelis Wynne 1797”. By 1838 the old church could not house the growing population. A new church, at a cost of £600, was started in 1838 and finished in 1839. The altar was set in one of the side walls with doors in the gables, as was the type of barn church common in Kilmore in the 19th century.

In 1866 the position of the high altar was changed to the end wall and the gallery was added at the other end. In 1870 a fine bell tower was added and in 1910 a new high altar was erected and a ceiling put in the church. In 1913 the church was heated and two carrera marble side altars were donated by parishioners. In 1951 the floor was tiled and new seats were donated by parishioners. Two stained glass windows in the end wall were also donated. In 1972 the church was re-modelled. The table of the altar was brought forward, the rails were removed and the wall panelled. The confessionals were removed and new ones built under the gallery which also had a new stairs erected.