The chair is named in honour of Bishop William Van Mildert, one of the founders of the university.
The holder of the Van Mildert chair, which is jointly funded by the university and Durham Cathedral, is also a residentiary canon at the cathedral and member of its Chapter, thus one of the requirements of post holder is to be an Anglican priest or a minister in another church in communion with Church of England.
The professor of divinity was one of the original chairs established at Durham University upon its foundation.
The first holder, in 1833, was Hugh James Rose, one of the founders of the Oxford Movement and later the second Principal of King's College London, but he resigned the post due to ill health after only a year, with the duties being taken on by Henry Jenkyns, the professor of Greek, with the assistance of Temple Chevallier, professor of mathematics, from 1835.
In 1839, the third prebendal stall at Durham Cathedral became vacant; this was attached to the chair of divinity (an arrangement made permanent by an Order in Council in 1841), allowing Jenkyns to resign the chair of Greek and take up the canonry and the professorship of divinity.