Clerk of the Rolls of the Isle of Man in the decades after Revestment, and steward of the Atholl manorial interests.

His patent for the office came from George III, reciting the King's confidence in the fidelity and prudent circumspection of his trusty and well-beloved John Quayle, and appointing him to hold the Clerkship of the Rolls during pleasure with all its rights, fees, profits and privileges.

The office made him the custodian of the Island's memory. When the Commissioners of Inquiry sat in 1791 and 1792 and wanted the record, it was Quayle who produced and certified it. Extracts from the Liber Scaccarii of 1641, 1690, 1707, 1719 and 1770, printed in the Commissioners' appendices, each close with his examination of the copy as Clerk of the Rolls. He was himself examined repeatedly at Douglas and Castletown through late September and October 1791, on the herring custom, on wrecks and flotsam, and on the constitution.

He also put his own view on paper. Writing from the Rolls Office at Castle Rushen on 17 October 1791, he told the Commissioners that he had carefully perused and considered Sir Wadsworth Busk's sketch of the history of the constitution and government of the Isle, that he believed it a just representation of facts, and that he concurred entirely with the Attorney-General in the principles and reasoning it advanced.

Alongside the public office he acted for the Atholl family. He and William Callow were appointed stewards of the manorial interests by the third Duke and continued under the fourth, remitting rents in bills through Drummonds and handling the mines, the impropriate tithes of Malew and the drafting of a proposed Act of Parliament on the ducal revenues. It fell to Quayle to report the death of Governor John Wood in a letter of 1 May 1777, noting that the Governor had been appointed by the Duke's grandfather and had remained a steady friend to the family.