A church was originally dedicated here in the 13th century by Bishop David de Bernham, but most sources agree that the current church likely dates from the early to mid eighteenth century, undoubtedly built on the site of an earlier ecclesiastical foundation most probably using materials from its predecessor building.

The church was extended to a T-plan in the 1840s when a North transept was added and further renovation took place in 1893 involving the introduction of a harmonium – courtesy of a Miss Lowson – to the right of the pulpit and replacing the old pulpit, as well as remodelling the entire building, with a Gothic style. This work was overseen by the Dundee-based architectural firm J. & F. Salmond.

The surrounding kirkyard is filled with many interesting gravestones and memorials and the most outstanding is the Aberlemno stone that is believed to depict the Pictish Battle of Nechtansmere on one side and a Celtic Cross on the other. This stone is a class II historical monument. These stones are covered up from September to April each year to protect them from the harsh Scottish winter but are still available to visit during that time.

The congregation of Aberlemno linked with the congregations of Rescobie and Guthrie Churches in 1983. In April 2024 the congregations of Aberlemno, Guthrie and Rescobie, Letham, Dunnichen and Kirkden, Lowson Memorial, and St Margaret Churches formed a union under Forfar All Souls Church of Scotland.