John Henderson was born at The Den Nursery, Brechin on 1 March 1804, the son of one of Lord Panmure’s gardeners at Brechin Castle, also John Henderson, and Agnes Thomson. He served his apprenticeship as a carpenter and after studying drawings and building construction and erecting the steeple of the parish church at Arbroath in 1831 spent some years as an assistant in the office of Thomas Hamilton until setting up on his own account in 1835. Much of his early work was in areas within Lord Panmure’s influence or from family connections. He appears to have taken on an assistant, John Nicol, in about 1833 who remained with him until about 1836 or 37.
Although expert in neo-Jacobean design from the start, Henderson’s neo-Gothic work was at first was of a very non-academic Georgian Gothic kind; but from 1843, when he received the commission for Trinity College Glenalmond, he became the foremost and for some years the only native-born exponent of Tractarian Gothic in Scotland, principally in the Early English and Mid Decorated styles. He was one of the eight applicants for the post of head of the Edinburgh office of the Office of Works in 1848, though without success.
Henderson died at 7 Greenhill Park on 27 June 1862 and was buried at Grange. His wife, Hannah Matilda Exley (born 1 January 1821 at Hull), whom he had married on 4 December 1843, survived him, dying in Edinburgh on 12 December 1894. Their son George, a sixteen-year-old apprentice at the time of his father’s death, was unable to continue the business. He completed his apprenticeship with David Cousin, a near-neighbour in Greenhill, who seems to have taken over at least some of the work in hand, though not the office records which were retained by his widow: Sir G G Scott took over at Glenalmond and, Cousin being a Free Church man, the Episcopal church building connection was lost to Scott’s pupil Robert Rowand Anderson.