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He was born at Bridge of Earn, Perthshire, and educated at the University of St Andrews and University of Edinburgh. In 1845 he became minister of St Paul's, Dundee, and in 1849 of Kettins, in Strathmore, where he remained for six years. In 1854 he was appointed Principal of St Mary's College, St Andrews. The appointment was immediately followed by the appearance of his Burnet prize essay on Theism. At St Andrews, where he was also professor of systematic theology and apologetics, his teaching was distinguished by several novel features. He lectured on comparative religion and treated doctrine historically, as being not a fixed product but a growth. Furthermore, Tulloch was appointed as one of Her Majesty's Chaplains for Scotland and preached a number of sermons before Her Majesty the Queen in Scotland between 1866 and 1876.
He quickly won the attachment and admiration of his students. In 1862 he was appointed a clerk of the General Assembly, and from then on he took a leading part in the councils of the Church of Scotland. Tulloch was also deeply interested in the reorganization of education in Scotland, both in school and university, and acted as one of the temporary board which settled the primary school system under the Education Act of 1872.
In 1878 he was chosen to be Moderator of the General Assembly, and did much to widen the national church. Two positions on which he repeatedly insisted took a firm hold—first, that a church must be comprehensive of various views and tendencies, and that a national church especially should seek to represent all the elements of the life of the nation; secondly, that subscription to a creed can bind no one to all its details, but only to the sum and substance, or the spirit, of the symbol.
For three years before his death he was convener of the church interests committee of the Church of Scotland, which had to deal with a great agitation for disestablishment. In 1884, he was a guest at Haddo House for a dinner hosted by John Hamilton-Gordon, 1st Marquess of Aberdeen and Temair in honour of William Ewart Gladstone on his tour of Scotland.  He died at Torquay, in 1886.
Tulloch's best-known works are collections of biographical sketches of the leaders of great movements in church history, such as the Reformation and Puritanism. His most important book, Rational Theology and Christian Philosophy (1872), is one in which the Cambridge Platonists and other leaders of dispassionate thought in the 17th century are similarly treated. He delivered the second series of the Croall lectures, on the Doctrine of Sin, which were afterwards published. He also published a small work, The Christ of the Gospels and the Christ of History, in which the views of Ernest Renan on the gospel history were dealt with; a monograph on Blaise Pascal for Blackwood's Foreign Classics series; and a little work, Beginning Life, addressed to young men, written at an earlier period.
A biography of Tulloch was written by Mrs Oliphant.
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- Beginning Life a Book for Young Men. 1882, ISBN Unavailable
- Modern Theories in Philosophy and Religion. Edinburgh and London: William Blackwood and Sons, 1884, ISBN Unavailable
- The Times, Monday, Feb 15, 1886; pg. 6; Issue 31683; col A Death Of Principal Tulloch.
- John Tulloch, Some Facts of Religion and of Life: Sermons Preached Before Her Majesty the Queen (Edinburgh and London: William Blackford and Sons, 1877)
- Emslie, Alfred Edward. "Dinner at Haddo House, 1884". National Portrait Gallery, London.
- This article incorporates text from a publication now in the public domain: Chisholm, Hugh, ed. (1911). "Tulloch, John". Encyclopædia Britannica (11th ed.). Cambridge University Press
- Tulloch, John, 1823-1886, Principal, St Mary's College, University of St Andrews, Scotland
- A memoire of the life of John Tulloch, Margaret Oliphant, 1888