Anderton was signed as an apprentice by Portsmouth manager Alan Ball, coming to prominence at 18 when he scored at Anfield in an FA Youth Cup match against Liverpool which ended 2–2. His first team debut came against Cardiff City in the second round of the League Cup in October 1990 as a substitute for youth team colleague Darryl Powell. Anderton made his full league debut against Wolverhampton Wanderers in a 0–0 draw, making 20 appearances in the 1990–91 season. Under new manager Jim Smith, Anderton became a regular in the attacking side of the 1991–92 season, scoring his first club goal in the season opener against Blackburn Rovers. His performances soon drew the attention of bigger clubs and after an impressive FA Cup run, during which he scored in a semi-final clash with Liverpool, he joined Tottenham Hotspur for £1.75 million in 1992.

After a slow start, Anderton settled at Tottenham, playing as a striker, forming part of an exciting attacking trio along with Teddy Sheringham and the young Nick Barmby. Two years later Terry Venables gave Anderton his England debut against Denmark in 1994. Anderton soon became a regular in the national side and turned down a move to Manchester United in the summer of 1995 following an exciting season spent playing with the likes of Jürgen Klinsmann at Tottenham, a decision that he later regretted.

Injuries then limited Anderton’s international appearances considerably. He missed most of the 1997–98 season but was recalled for Glenn Hoddle’s squad for the 1998 FIFA World Cup in France, starting on the right wing in the first two matches ahead of an out-of-sorts David Beckham. Hoddle later said in his World Cup Diary that he thought Anderton was equally as good as Beckham at crossing and was a better defender. Hoddle said he had waited 18 months to play Beckham and Anderton together on the right side of midfield. It finally happened as David Batty was dropped and the now-focused Beckham was recalled for the third game against Colombia and played inside of Anderton. Anderton and Beckham were the England heroes as they both scored spectacular goals. In the second round against Argentina, England went on to lose on penalties. The following year Anderton won the League Cup with Tottenham, and signed a new reported £24,000-week contract in March. After being sidelined during Euro 2000 with an Achilles tendon injury, an extended run of fitness saw Anderton vying for a permanent place in the national team again. He played in England’s 1–1 draw away to France in September 2000 and also featured against Italy the following November.

In the summer of 2001 Anderton was heavily linked with a move to Liverpool but he remained at Tottenham and his good form for Glenn Hoddle’s team during the early part of the 2001–02 season earned his first call-up to Sven-Göran Eriksson’s England squad for a friendly against Sweden in November. Anderton was again selected by Eriksson for England’s next game, a friendly against Holland, in February 2002. He would have started the game but was forced to withdraw through injury. One notable statistic about Anderton’s England career is that his last five caps were given to him by five different managers. These were: vs Czech Republic (18 November 1998) by Glenn Hoddle, vs France (10 February 1999) by Howard Wilkinson, vs France (2 September 2000) by Kevin Keegan, vs Italy (15 November 2000) by Peter Taylor and vs Sweden (10 November 2001) by Sven-Göran Eriksson.

On 8 September 2006, Anderton joined League One club AFC Bournemouth on a ‘pay-as-you-play’ basis, scoring a spectacular 40-yard free kick on his first-team debut against Scunthorpe. On 10 February 2007, he scored his first career hat-trick against Leyton Orient. Following a pre-season friendly with Portsmouth in July 2007, Portsmouth boss Harry Redknapp heaped praise on Anderton, telling the Bournemouth Daily Echo: “In the right team and with the right players around him, I honestly think he could still be playing in the Premiership”.

Anderton signed a new one-year contract with Bournemouth at the start of the 2008/09 season which would have taken him past his 37th birthday. However, on 4 December 2008, Anderton announced he would retire on 7 December 2008, one day after his last game for club against Chester City. In his last match, versus Chester, Anderton bowed out of football with a fairytale finish, as he scored the winning goal with a spectacular volley in the 88th minute after coming on as a substitute in the second half of the game.

Anderton has worked as the in-studio analyst for Canadian network TSN’s coverage of Euro 2012. In 2013, he was unveiled as the honorary president of Arlington Spurs [1], a Tottenham Hotspur supporters club based in Arlington, Virginia, USA.