The congregation originates from the efforts to bring the Gospel to the Gaelic-speaking Highlanders in Edinburgh in the 18th century. The congregation in the Gaelic Chapel came out with the Free Church at the Disruption and built a church in Cambridge Street. In 1864 the name was changed to St. Columba’s. Only a tiny minority of that congregation remained out of the Union of 1900. When the Free Church was allocated St. John’s church (built for the congregation of the Disruption minister, Dr. Thomas Guthrie) in 1907 for their Assembly Hall, that building also became the home of the St. Columba’s congregation.

In 2011 a new place of worship, a building belonging to the City Mission, was purchased by the congregation.