Margetson began his career with Manchester City, signing as a YTS trainee at the age of 18 where he featured largely as understudy during a downturn in the club's fortunes.

[2] Despite performing well in the run-in to the club's relegation battle to the 3rd-tier of English football in 1998, he was guilty of picking up a back pass to concede a free-kick inside the penalty area against Queens Park Rangers.

Margetson moved on at the end of season on a free transfer for a spell with Southend United, making his debut on 8 August 1998 in a 2–1 victory over Scarborough.

[7] He joined Cardiff City on trial during a pre-season tour in Scotland,[8] before eventually signing a permanent deal at Ninian Park.

[15] He remained as back-up to Neil Alexander throughout the season and announced his retirement at the end of year, becoming the club's full-time goalkeeper coach.

An unused substitute against Norway, Margetson was handed his international debut on 30 May 2004 when he replaced Danny Coyne at half-time during a 1–0 win over Canada.

[25] In August 2016, Margetson stepped down from his role with Wales to join the England national football team coaching staff, following the appointment of Sam Allardyce.

[29] Margetson joined Swansea City in June 2019 as the club's new goalkeeping coach, which he performed alongside his role with the England national team.