As a young barrister, John Eardley Wilmot was taken up by Charles Talbot, 1st Baron Talbot, who was Lord Chancellor from 1733 to 1737, Philip Yorke, 1st Earl of Hardwicke, the next Lord Chancellor, 1737 to 1756, and Sir Dudley Ryder, an Attorney General and Lord Chief Justice. Bishop John Hough of Worcester wrote to Wilmot's aunt on 4 May 1737:
|“||I hear every body speak of your nephew Wilmot, as one of the most hopeful young gentlemen at the Bar... he may, without presumption aspire to any thing in the course of his profession; and has no small encouragement from what he has seen, since his acquaintance with Westminster-hall, in four or five of the long Robe, who have reached the top in the prime of their years.||”|
He joined the Midland Circuit and was an advocate at the Derby Assizes. Dudley Ryder appointed Wilmot a junior counsel to the Treasury, and in 1753 he was offered promotion to King's Counsel and to serjeant-at-law, but declined and returned to Derbyshire. However, in February 1755 he accepted the appointment as a judge of the King's Bench and serjeant-at-law, and was knighted. In 1756, he became a Commissioner of the Great Seal and was proposed as Lord Chancellor, but said he didn't want it.
William Blackstone, author of the famous Commentaries on the Laws of England (four volumes, 1765–1769) was one of Wilmot's close friends. Blackstone wrote to him on 22 February 1766, after the publication of the first volume of the Commentaries: "Sir, Lord Mansfield did me the honour to inform me, that both you and himself had been so obliging as to mark out a few of the many errors, which I am sensible are to be met with in the Book which I lately published. Nothing can flatter me so much as that you have thought it worth the pains of such a revisal."
In August 1766, Wilmot became Chief Justice of the Common Pleas, and in September 1766 joined the Privy Council. In 1770, he again refused appointment as Lord Chancellor, and in January 1771 resigned as Chief Justice.
In the aftermath of the American Revolutionary War, Wilmot was appointed as a royal commissioner to investigate claims by American Loyalists for compensation for the losses they had suffered as a result of the war.
He died in London in 1792 and was buried at Berkswell, Warwickshire, a country estate which had been inherited by his wife.
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