Dion Dublin was released by Norwich without ever making a first team appearance although he played six times for the Reserves. He joined Kings Lynn before moving onto Cambridge United where his goals (52 in 156 games) helped his side threaten to claim a place in the top flight. Signed by Manchester United for £1million in 1992, he made twelve appearances for the Red Devils scoring twice. Sold to Coventry City, he has played both as a central forward and as a centre-half.

Dion made his 100th league appearance for Coventry on the first day of the 1997/98 season. He marked this occasion with a hat-trick to give Coventry a 3-2 victory over the highly fancied Chelsea. The Sun speculated on 17th December 1997 that Dublin was a target for Bryan Robson's Middlesbrough. Leicester City and Crystal Palace were also rumoured to be interested as Coventry sought to regain some of their money spent on Romanian international striker Moldovan. Dion's impressive form for Coventry City earned him a surprise call-up to Glen Hoddle's England squad for the pre-World Cup friendly against Chile in February 1998 and made his debut in the 2-0 defeat. He seemed to jump above Robbie Fowler, Stan Collymore, Emile Heskey and Chris Sutton in England's pecking order. As transfer deadline day approached, Dion was linked with £ 5million moves to Blackburn and Liverpool (who supposedly were keen on his defensive abilities).

The end of the season saw Dion finish joint top Premiership marksman. His 18 goals being equaled by Chris Sutton and Liverpool's Michael Owen. This resulted in increased transfer speculation with champions Arsenal the media's favourite for Dublin's next destination. According to the Daily Mirror, new Newcastle boss Ruud Gullit has supposedly made a £7million bid for Dion to partner Alan Shearer. The News of the World reported on October 25th 1998 that Blackburn are lining up a £6million bid for Dublin who is supposedly angry with Coventry about new book "Staying Up" written with the approval and co-operation of Coventry chairman Bryan Richardson. In one section, Richardson is involved in alight-hearted conversation with Manchester United manager Alex Ferguson over the size of Dublin's manhood. Although Coventry and Blackburn agreed a £6.75million transfer, Newcastle, Leeds and Aston Villa entered the race making improved offers for Dion's services.

Despite better personal terms offered by Newcastle and Blackburn, Dion opted for Aston Villa so not to disrupt his family as they could stay in the Midlands. He transferred eventually for £5.75 million and made his debut for Villa in the 3-2 home victory over Tottenham on 7th November 1998 where Dion scored twice. A hat trick followed in his second game which was a 4-1 victory over Southampton before getting two in Villa's 4-2 defeat at home to Liverpool. He could have scored a hat-trick for the second week running but his penalty was saved by David James. In between the Southampton and Liverpool games, Dion started for England in their 2-0 victory over the Czech Republic and had an impressive game, suggesting that he might partner Michael Owen in the next England game at the expense of Alan Shearer. Not bad for a Norwich City reject.

In December 1999, it was reported by the News of the World that Villa manager John Gregory's £40million expenditure on the transfer market was deemed unacceptable by the club's board who saw the value of their shares plummit. Although Gregory has supported Dublin's claims to an England place as Kevin Keegan had left him out of his England squads, the papers speculated that Dublin would be sold for £6million to help reduce the transfer deficit. Any plans were overshadowed in December 1999 when Dion suffered a life threatening broken neck in a clash with Sheffield Wednesday. There were doubts over whether he would ever play again but he proved them wrong and made a miraculous return to the Villa team on 25th March 2000 coming on as substitute against Derby, albeit with a metal plate fusing together three vertebrae. The following week he came on as substitute in Villa's FA Cup semifinal against Bolton and completed the fairytale by scoring Villa's 4th penalty against Jussi Jaaskelainen thus sending Villa to the final. Unfortunately for Dion and Villa, the Villa side did not play particularly well in the Final on 20th May and lost 1-0 to Chelsea.

On 23rd July 2000, The Sunday People reported that Middlesboro boss Bryan Robson was preparing a £8million bid for Dublin. Robson was said to be seeking firepower in his challenge to take Boro into Europe and had £15million to spend. Dion's poor scoring record in 2000/01 and the £9.5m signing of Colombian striker Juan Pablo Angel in December 2000 suggests that Dion's career at Villa Park might be coming to an end. Leicester manager Peter Taylor is said by Teamtalk to be watching the situation closely. On 22nd July 2001, Crystal Palace manager Steve Bruce was said to have bid £1.5million for Dion's service. Dion was also said to be on Gary Megson's shopping list as he sought to replace Lee Hughes who joined Coventry for £5million in the summer of 2001. A move to Filbert Street was suggested again at the end of January 2002. February 2002 saw rumours that ambitious Welsh side Cardiff City had approached Villa to take Dion on loan but this rumour was dismissed by Villa.

Displaced even further by Graham Taylor's signing of Peter Crouch from Portsmouth, Dion was allowed to join Millwall on loan on Transfer Deadline Day 2002 (28/03/02), with him due to stay at the New Den until the end of the season. Prior to Millwall's visit to Highfield Road on 12th April 2002, Coventry manager Roland Nilsson announced that he would love to bring Dion back to Coventry in the summer. "I don't know whether Dion would want to play in the First Division or come back to his old club but it is something we will look into, and if it is the case, maybe we can do something." Dion's form with Millwall saw them linked with a permanent move for him if they gained promotion to the Premiership. However Southampton were also said to be keen. Millwall's play-off semi-final defeat saw Dion return to Villa where his chances looked even slimmer following the signing of Swedish striker Marcus Allback. The Sunday People claimed on 19 May 2002 that Dublin would join Spanish side Tenerife, accompanined by veteran Arsenal and England defender Martin Keown. Wolves have also been linked with Dublin whilst the Daily Express speculated on 25th July that Portsmouth would swoop for the versatile veteran.

On Sunday 22nd September 2002, the Sunday People claimed that Walsall were planning to take Dublin and Villa teammate Steve Stone to the Bescot Stadium on a three month loan deal. Dublin obviously wasn't impressed with this idea as he placed himself firmly back into Graham Taylor's first team plans by scoring the winner that day in the 3-2 victory over Everton. A turbulent season followed including a sending-off for headbutting Robbie Savage. Allegedly Dublin's agent was hawking him around a number of clubs and Portsmouth showed an interest in signing him in the summer of 2003. However rumours from the Midlands have linked him with a return to Highfield Road.

Following the sale of Rotherham striker Alan Lee to Cardiff at the beginning of the 2003/04 season, Rotherham manager Ronnie Moore is alleged to have approached Villa about taking Dion on loan to Millmoor for the remainder of the season. Rumours suggested that Norwich approached David O'Leary about bringing Dublin on loan to Norwich. This was denied by both parties. Burnley hoped to bring Dublin to Turf Moor as a replacement for Forest-bound Gareth Taylor but O'Leary was unwilling to lose another striker after Peter Crouch's loan to Norwich. The following week saw rumours that Barnsley manager Gudjon Thordarson had been scouting Dublin in preparation for a transfer bid.

In January 2004, the Scottish media amazingly speculated that Rangers were hoping to sign 34 year old Dublin on a two year deal as Alex McLeish was impressed by his versatility - Dublin can play as centre-back or centre-forward. In May 2004, it was suggested that Dion might return to Coventry City as one of Peter Reid's first signings for the Highfield Road side. Dion was given a free transfer on May 14th 2004 and has been linked with both Leicester and Derby, in addition to Coventry with Peter Reid confirming their interest in signing Dion. At the end of the month, speculation in the media linked Dion with troubled Leeds United.

Reports in early June suggested that Dion had agreed to join his hometown club Leicester City. Micky Adams, their manager, said "Dion will bring a massive wealth of experience and will help in our bid to get back into the Premiership ..He is a model professional and provides opportunities for us in both attack and defence."

Following the sacking of Cambridge's French manager Herve Renard in December 2004, Cambridge chairman Gary Harwood admitted he would like to bring
U's legend Dion Dublin to the club as their new manager. Dion was not in new Leicester manager Craig Levein's plans. "We are in no rush to recruit the right man for the job but if Dion is interested, we would certainly be interested in hearing from him,'' said Harwood. "Dion had a memorable time here and I would certainly not rule out holding an interview with him to see what he has got to say. "His appointment would certainly be popular and he would also add valuable experience - and possibly get us a few goals while he is at it."

Speculation in the Sunday papers on 1st January 2006 suggested that Dion would be released / free to leave Leicester during the January 2006 transfer window - although another report suggested he might replace Craig Levein as the Foxes' manager. Although Levein was sacked during January 2006, Dion also departed the club leaving on a free transfer on 30th January and joined former manager Gordon Strachan at Celtic on a short term contract.

Released by Celtic at the end of the 2005/6 season, Dion trained with Leicester whilst seeking a new club. He joined Norwich on 20th September 2006 as a free agent and made his debut in the 3-1 away defeat to Plymouth on 23rd September 2006. He scored his first professional goal for the Canaries in the 3-3 draw at QPR on 14th October 2006.

Impressing during the 2006/7 season, Dion was offered a one year extension to his contract in April 2007 but didn't sign it immediately stating that he had to think about the travelling time from his home in the Midlands and the impact on his family. Whilst deliberating on the offer from Norwich, Peterborough United made an approach to take Dublin to London Road where he would link again with former Old Trafford teammate Darren Ferguson.

In January 2008, Dion announced his retirement at the end of the 2007/8 season and was quickly approached by non-leaguers Lowestoft Town. Dion made his last appearance at Carrow Road on 26th April 2008 when he came on as a substitute for Jamie Cureton in the 3-0 win over QPR that secured Norwich's place in the Championship. On the same day, he was awarded the Player of the Season Award for 2007/8.

Since retiring, Dublin has worked in the media as a pundit for Sky Sports. As well as appearing on Ford Super Sunday with Richard Keys, Dublin has done commentary on a number of games including the UEFA Champions League games with Martin Tyler. He has also co-presented 606 on BBC Radio 5live. Away from football he has invented a unique percussion instrument called The Dube.

In January 2011, it was announced that Dublin, along with former Ipswich player Matt Holland, would host BBC One’s popular Football League magazine show Late Kick Off

In March 2015, it was announced that Dublin would co-host property programme Homes Under The Hammer.

He was appointed as a member of Cambridge United's board of directors in July 2021. He said “It must have taken me about five seconds to say yes. I’ve had lots of conversations with Shaun (Grady) and Godric (Smith) about how it can work with my input. I’m just very happy to be part of the football club that helped me many years ago. Having been in some really successful dressing rooms and situations with the club, it felt right to try and help them moving forward. They’re doing great as it is, but to be part of some big decisions will be nice. Everybody knows that I’ve got other jobs to do, but being asked to do a job like this, I was never going to turn it down, and I feel quite privileged to be asked to do it.”