Watkin made his first-class debut against Worcestershire in 1986, taking the wickets of Graeme Hick and Phil Neale, and also played two Sunday League games, but had to wait until 1988 for a second chance. That year he established himself as an important member of the Glamorgan first team, taking 8 for 59 (which was to remain his career best) against Warwickshire, and claiming 46 first-class scalps in all that season. His best year in terms of wickets was 1989, when he captured 94, and in his career he took a total of 902 wickets.

He made his England Test debut unexpectedly in 1991, when Chris Lewis pulled out on the morning of the first test against the West Indies. Watkin's bowling was ideal for Headingley's notorious seamer friendly conditions. Watkin took five wickets, including those of Carl Hooper, Viv Richards and Gus Logie in a match-turning spell in the second innings, in England's ultimate victory in the match, but he fared less well two weeks later at Lord's, where his only significant contribution was to hang around for nearly an hour with the bat while Robin Smith played the best innings of his career at the other end. He returned to the Test team for the Sixth Test in 1993, when he took six wickets, including the first three of Australia's second innings, in England's only victory of the series.^[3] He was selected for the subsequent tour of the West Indies, but did not play in any of the Tests: he perhaps would have held his place for the First Test, but suffered back trouble which put him out of the side, Alan Igglesden playing in his place. He did play in four of the five ODIs on that tour, bowling particularly creditably in the 2nd in Kingston, Jamaica, with four wickets on his comeback after missing the 1st Test: but a loss of form in the later ODIs and a subsequent recurrence of his back problem cut his tour short, the only time injury got the better of him in his career. He was not considered for international selection again, although some considered him unlucky in this regard.

In 1998, Watkin was given a benefit by Glamorgan, which raised £133,000. Normally a poor batsman, he managed to average a startling 35.66 that year, despite a top score of just 25, thanks to 13 not outs in his sixteen innings. By contrast, his career average was 10.83.^[4] In 2000, he scored 51 against Gloucestershire, the only half-century of his career.

After retirement in 2001, Watkin became Director of the Welsh Cricket Academy.