[5][6] Having started his career with Watford, James went on to feature in the Premier League for Liverpool, Aston Villa, West Ham United, Manchester City and Portsmouth.

[13] Following the departure of Tony Coton, James made his league debut on 25 August 1990 in a 1–2 defeat against Millwall, and his performance resulted in an England U21 call-up for a match against the Republic of Ireland.

[16] After conceding twenty goals in eleven matches in the first half of the 1993–94, he was dropped in favour of veteran Bruce Grobbelaar, but was recalled to the starting line-up and kept his first clean sheet of the season in a 1–0 away win over Arsenal on 31 January 1993, which included a penalty save from Paul Merson.

[19] James made his Villa debut on 7 August 1999, and kept a clean sheet in a 1–0 away win over Newcastle United in the opening Premier League game.

He was decisive in a penalty shoot-out against Bolton Wanderers in the 2000 FA Cup semi-final, but conceded Chelsea's winning goal in the ensuing final, the last to be staged at the old Wembley.

James stayed with West Ham at the start of the 2003–04 season before returning to the Premier League, signing for Manchester City on 14 January 2004 for an undisclosed fee as a replacement for the retired David Seaman.

There were still two minutes of normal time remaining, plus five for stoppages, when [manager] Stuart Pearce, adopting a form of leadership that would have been wacky even by Brian Clough's standards, had the brainwave of replacing a midfielder, Claudio Reyna, with his reserve goalkeeper, Nicky Weaver, and ordering David James to play as a centre-forward.

With James charging around like a headless ostrich, his cameo role incorporating a hilarious air-shot and at least two horrendously late but probably well-meant chops at Doriva's legs, the hitherto wretched referee Rob Styles decreed that Joey Barton's centre had flicked off Franck Queudrue's hand for a penalty."

With five minutes remaining the score was 1–1, when City's manager Stuart Pearce replaced midfielder Claudio Reyna with the substitute goalkeeper Nicky Weaver, and James was moved to play in attack for the remainder of the game.

The unusual tactic almost worked when, in injury time, Middlesbrough defender Franck Queudrue conceded a penalty by handling a cross that was aimed at James.

However, Robbie Fowler's penalty was saved by Middlesbrough goalkeeper Mark Schwarzer, meaning they qualified for the UEFA Cup at City's expense.

[33] On 22 April 2007, James kept his 142nd Premier League clean sheet in a goalless draw with Aston Villa, breaking the record of 141 previously held by David Seaman.

[37] James won the second major trophy of his career during that season, as Portsmouth claimed a 1–0 victory over Cardiff City at Wembley Stadium in the 2008 FA Cup Final.

[45] He stated that he hoped that his performances at the club would keep him on the radar for the England team and that his decision to join them was motivated by a desire to be closer to his family home in Devon.

[48] On 10 March 2012, James reached 900 club appearances in a game against Cardiff City in the Severnside derby, in which he was made captain as a mark of respect.

The ÍBV chairman stated that James was not being paid high wages, and that he was primarily playing out of kindness and to gain coaching experience.

He kept his first international clean sheet as England beat Mexico 2–0 with goals from Teddy Sheringham and James' Liverpool teammate Robbie Fowler.

James came on as a half-time substitute and conceded all four goals in the 4–1 drubbing England suffered at the hands of Denmark during a friendly on 17 August 2005 – their worst defeat in 25 years.

Along with fellow veterans David Beckham and Sol Campbell, James was dropped from the England squad at the start of Steve McClaren's reign and was not called up during the 2006–07 season.

[71] Prior to the tournament, James was backed to reclaim the number one shirt by former England goalkeepers Gordon Banks[72] and David Seaman.

Following his stint at ÍBV, James joined Luton Town in October 2013 in a coaching capacity in order to gain experience towards a UEFA A-licence qualification.

[58] Utilising a distinctly British identity, signing players such as Stephen Pearson and Michael Chopra, he took them to the ISL playoffs at the first attempt, after a 4th-place finish in the league phase.

In the playoffs, extra time was needed to see off Chennaiyin 4–3 on aggregate, taking James and Kerala Blasters to the 2014 Indian Super League final, only to lose 1–0 to Atlético de Kolkata.

James returned to the helm of the club as their head coach a day after the sacking of Rene Meulensteen on 3 January 2018, following a string of poor performances.

[9] He set about rebuilding the side in the January transfer window, releasing Mark Sifneos and signing Iceland international midfielder Guðjón Baldvinsson on loan from Stjarnan, along with appointing former Portsmouth teammate Hermann Hreiðarsson as his assistant.

In May 2007, a "Who Ate All the Pies" column ridiculed him, among David Beckham and others,[96] for "backcombed efforts",[97] and likened a previous November 2006 cut to fictional character Clark Kent,[98] both captured by BBC Match of the Day.

[101] He subsequently set up the David James Foundation in order to help maize farmers in Malawi develop more efficient production techniques.

Despite earning an estimated £20m from his footballing career, owning several properties and having a lucrative contract modeling for Armani, James' debts had built up since his divorce from his wife, Tanya, in 2005.

Items included 150 signed shirts, shorts and match balls as well as his customised Vauxhall Astra van and Raleigh Chopper bikes.

[130] In November 2024, James was announced to be a contestant in the 2025 Taskmaster's New Year Treat special episode, alongside Hannah Fry, Martin Lewis, Melanie Blatt, and Sue Johnston.