The church was built by Neil Malcolm of Poltalloch in the policies of his new mansion at Calton Mor, and was completed and consecrated in 1854. He settled an endowment for the stipend of the Incumbent and for maintenance of the building. The graveyard is a private burial ground.
The architect of the church was Thomas Cundy, Junior. He was surveyor of the Grosvenor Estate in London during the development of the residential area of Belgravia, and designed several London churches, including St Paul’s, Knightsbridge, and St Barnabas’, Pimlico. This is his only work in Scotland.
St Columba’s is a notable exemplar of the principles of the Cambridge Camden Society, both in design and detail. There is a full set of stained-glass windows by William Wailes.
The charge was an Independent Incumbency from 1854 to 1934, held jointly with Christ Church, Lochgilphead from 1927. From 1934 till the war there were regular services only in August and September, conducted by visiting clergymen. From the outbreak of war in September 1939, Sir Ian Malcolm of Poltalloch, a lay reader, conducted evensong every Sunday for three years with scarcely a break, himself preaching the sermon and playing the organ; the average attendance was thirty people. The church was unused from 1943 to 1947. Since then the Rector of Christ Church, Lochgilphead, has been priest-in-charge, and there have been services on two Sundays each month.
In 1917 the endowment was conveyed to the Representative Church Council, the Laird of Poltalloch remaining patron.
The rectors lived at Duntrune Castle until 1917 and thereafter at Lower Raslie.