John Popham married very young, apparently when no more than 17; his wife, who was heir to the manor of Castleton in Glamorganshire, may have been a ward of his father, from whom John was to inherit property in Bridgwater, Somerset. According to Aubrey it was not until he was 30 years old that Popham was persuaded by his wife to concentrate on his legal studies. He had earlier been put out of commons by his inn, where in November 1556 he was restored on paying a fine of 40s.; and it was not until the 1560s that he began that progress which brought him to the top of his chosen profession.3CPR, 1553, p. 326; Manning, Speakers, 247; C142/108/104; M.T. Recs. i. passim.
Popham’s election to the Parliament of 1558 by Lyme Regis may have been the work of his brother-in-law William Pole, who sat for the town in 1545 and who was to become its legal counsellor. Nothing is known of Popham’s role in Mary’s last Parliament although his name is marked with a circle on a copy of the list of its Members in use for the second session: the significance of the circle has yet to be explained.4Wm. Salt Lib. SMS 264.
After a long and distinguished career under Elizabeth, Popham died on 10 June 1607, and was buried in the church at Wellington. Several portraits of him in middle age survive.5Collinson, ii. 483; Cat. Boughton House State Rooms and High Pavilion, 1, 2.