Conant quickly gained a mastery of Greek, debating publicly in that language, and also excelled in Hebrew, Syriac, and Arabic.
John Conant graduated BA on 26 May 1631, and MA on 12 January 1634; on 30 June 1632 he was chosen a probationer of Exeter College, and on 3 July 1633 made a fellow.
He was ordained deacon and tutored pupils until 1642, when the disruption of Oxford by the Civil War forced him to depart, abandoning valuable books, which he never regained.
There his uncle preached to the House of Commons on 26 July 1643, calling on it to reform the church, and he was a member of the Westminster assembly (not the nephew, as some sources incorrectly assert).
Lady Chandos, the daughter of Henry Montagu, Earl of Manchester, was his patron, awarding him an annual stipend of £80, much of which he used to relieve the poor and needy of the parish, and provide them with bibles and schooling.
In 1649, when George Hakewill the Rector of Exeter College died, a majority of the fellows wanted Conant's uncle for the position, but the elder Conant, wishing to remain at the parish of St Thomas, Salisbury, urged his nephew for the post; the nephew was duly elected on 7 June 1649, and admitted to the office on 29 June 1649.
Conant was presbyterially ordained to the ministry at Salisbury in October 1652, and in September 1654 he was appointed Regius Professor of Divinity at Oxford.
Shortly after Richard Cromwell succeeded his father as chancellor of Oxford University, he named John Conant as vice-chancellor, on 9 October 1657.
While vice-chancellor, Conant restored many traditions, such as the wearing of caps and hoods, which his predecessor John Owen had considered popish.