He was admitted a student of Lincoln's Inn on 15 March 1639, and, having been called to the bar in 1647, practised in the Court of Chancery, where he acquired an extensive business.
Roger North relates that he 'heard Sir John Churchill, a famous chancery practiser, say, that in his walk from Lincoln's Inn down to the Temple Hall, where (in the Lord Keeper Bridgman's time) causes and motions (out of term) were heard, he had taken with breviates, only for motions and defences for hastening and retarding hearings'.
Churchill was knighted on 16 August 1670, and appointed autumn reader at Lincoln's Inn in the same year.
The quarrel between the two houses was at length put an end to by the prorogation of parliament by the king on 9 June, when Churchill was immediately released.
The manor of Churchill in Somerset, which he purchased from Richard Jennyns, was sold soon after his death for the payment of his debts.