He held a number of offices, including Chancellor of the Duchy of Lancaster (1542–1547), Comptroller of the Household (1540–1547), Constable of the Tower (1540–1556) and Lord Chamberlain (1553–1556).

John Gage was born on 28 October 1479 at Burstow manor in Surrey and baptized at the parish church there on the same day.

Present at the funeral of Henry VIII, he was appointed one of the executors of the king's will and a member of Edward VI's Regency Council.

Their alabaster altar tomb in the north chapel of that church is the work of Gerard Johnson the elder (1541–1611) and, along with monuments for some other members of their family, was erected in about 1595.

A lengthy and detailed household inventory was added as a schedule to the will and points to the wealth and lifestyle that Sir John enjoyed.