After leaving Manchester United at the end of the 2000–01 season, Sheringham re-joined Tottenham Hotspur, where he was a losing finalist in the 2001–02 Football League Cup.

After being loaned out by the club twice in 1985 to Aldershot and later a Swedish side, Djurgården, he quickly became a first choice selection at Millwall and during the late 1980s formed a striking partnership with Tony Cascarino.

He did well for Forest and helped them finish eighth in the First Division at the end of the 1991–92 season, as well as to reach the League Cup final, where they lost to Manchester United.

Sheringham had a successful start to his career at the club by being the Premier League's top goalscorer in its inaugural season, scoring 22 goals (21 with Tottenham and one with Forest).

[15] His strike partners at White Hart Lane included Gordon Durie, Ronny Rosenthal, Jürgen Klinsmann and finally Chris Armstrong.

Sheringham scored 14 goals in all competitions and formed a good partnership with Andy Cole but the 1997–98 season ended without the league title.

Towards the end of the season, during a game at Bolton Wanderers, an incident occurred that furthered the animosity with fellow striker Andy Cole.

[20] Speculation that Sheringham would leave United increased just after the 1998–99 season got underway, when Dwight Yorke moved to Old Trafford from Aston Villa.

Yorke immediately formed a prolific partnership with Cole as United went on to regain the league title on the final day of the season.

Sheringham's first-team chances were relatively limited but he still managed to make enough appearances to qualify for a championship medal at the end of the season – at the age of 33 he had won his first major trophy.

[21] Four days after the FA Cup triumph, Sheringham scored a dramatic stoppage-time equaliser against Bayern Munich in the Champions League final, having come on as a substitute earlier in the game.

[22] Sheringham's first-team chances remained limited during the 1999–2000 season, but he still played enough times to merit another Premier League title medal.

[39] With his second-half appearance against Charlton Athletic on 2 April 2006, Sheringham became one of just five players to have played top-flight football while in their 40s; joining the likes of Les Sealey, John Burridge, Gordon Strachan and later Ryan Giggs.

On 26 December 2006, at the age of 40 years and 266 days, he beat his own record for oldest Premier League scorer, with the goal in a 2–1 defeat to Portsmouth.

[43] On 30 December 2006, he broke the record for oldest Premier League outfield player once more, playing in the 1–0 defeat against Manchester City, aged 40 years and 270 days.

At this time, the England squad were also criticised heavily in the media for their part in several off the field incidents during the lead up to the tournament, where Sheringham, McManaman and Gascoigne were photographed drinking heavily and playing "dentist chair" drinking games as well as destroying the first class cabin of a Cathay Pacific flight which went down poorly with the public.

[55][56] Sheringham continued to be a first choice selection under new England manager Glenn Hoddle (1996–99) until the emergence of new teenage superstar Michael Owen during the course of 1998 saw him overshadowed.

He was often deployed as a tactical substitute late in games by Eriksson, valued for his ability to hold the ball up and create intelligent play.

In 2001, Sheringham scored an important goal for England against Greece in a World Cup qualifying match within 15 seconds of coming on as a substitute, although this event is overshadowed by the 93rd minute equalising free-kick by David Beckham.

[57] He was selected as part of Eriksson's 2002 FIFA World Cup squad after impressing throughout the 2001–02 season with his club, and played in the famous 1–0 win against Argentina, almost scoring a goal with a volley that was well saved by the Argentine goalkeeper, and made his final England appearance as a substitute in the 2–1 quarter-final defeat to Brazil in Japan.

[58] At the age of 36, that defeat signalled the final end of Sheringham's international career, during which he had earned fifty-one caps and scored eleven times for England.

[62][63][64] As a centre-forward in his prime, he was also very effective and extremely prolific, due to his accurate finishing, opportunism in the area, intelligence, and his ability in the air, which enabled him to be regarded as one of the top Premier League forwards of his generation.

[60][65] Upon his retirement from professional football in 2008, Sheringham has been a noticeable figure on the world poker scene,[66] playing in various competitions worldwide.

He made the final table in the €5,000 No Limit Hold'em Main Event in the EPT Vilamoura, finishing 5th out of a field of 384 players, winning €93,121.

[68] He was credited with a change in West Ham's style of play which led to a run of good form at the start of the 2014–15 season, earning striker Diafra Sakho the Premier League Player of the Month award for October 2014.

[69] On 21 May 2015, Sheringham was appointed to his first managerial role, taking charge of League Two side Stevenage, replacing Graham Westley.

[70] With the club struggling with injuries, he registered himself as a player, aged 49, for a Herts Senior Cup match against Welwyn Garden City in November of that year, but did not play.