Cunningham was born in Hamilton, Lanarkshire and studied at the University of Edinburgh. He was ordained a minister in the Church of Scotland, and in 1830 was ordained to a collegiate charge in Greenock, where he remained for three years. In 1834 he was transferred to the charge of Trinity College Kirk, Edinburgh. His removal coincided with the commencement of the period known in Scottish ecclesiastical history as the Ten Years' Conflict, and he left the Church of Scotland in the Disruption of 1843 to become one of the founders of the Free Church of Scotland, alongside Thomas Chalmers and Robert Smith Candlish. Towards the end of 1843 he visited America to make the case for the Free Church and he raised some money there, having already received the degree of D.D. from Princeton University. Cunningham was appointed Professor of Theology at the New College, Edinburgh, before transferring to the chair of Church History in 1845, replacing Rev David Welsh. He succeeded Thomas Chalmers as Principal in 1847, serving in that position until his death, and was appointed moderator of the Free Church General Assembly in 1859. Cunningham specialised in historical theology, and wrote a two volume work on the subject. An open source audio narration of the book is available. He also wrote The Reformers and the Theology of the Reformation. William Garden Blaikie suggested that he was the "ablest defender of Calvinism in his day" and that the "gentleness of his personal character was a striking contrast to his boldness and vehemency in controversy." Cunniingham has been described as a scholar and controversialist. According to the Encyclopædia Britannica Eleventh Edition, "his... sympathies combined with his evident desire to be rigidly impartial qualifying him to be an interesting delineator of the more stirring periods of church history, and a skilful disentangler of the knotty points in theological polemics." In later life Cunningham lived at 17Salisbury Road in south Edinburgh. He died in Edinburgh and is buried beneath a large sarcophagus-style grave in the Grange Cemetery alongside the north path.
