Dan Ashworth began his career with Norwich City. He later played for St Leonards and coached in the USA with the West Florida Fury before returning to East Anglia to sign for Wisbech

Wisbech's dire financial situation in the autumn of 2000 led to drastic wage cuts. Dan took this opportunity to leave the Fenman along with 5 other players (Paul Hill, Ian Pledger, Andy Gleave, Ricky Hailstone and Matt Carmichael)

Dan was promoted from Education and Welfare Officer to Academy Director at Peterborough following the Posh youngsters' poor start to the 2000/01 season. He replaced Adrian Boothroyd who was demoted to managing the 8-16 year olds. Dan worked closely with Kit Carson. In addition, Dan continued his playing career by signing for Eastern Counties League side Diss Town

Following Kit Carson's departure from London Road, Dan also left and joined rivals Cambridge United who ironically appointed Carson as Head of Youth Development in November 2001.

In February 2004, Dan left Cambridge to assist Adrian Boothroyd in setting up West Bromwich Albion's Academy. He was later appointed as Technical Director in December 2007. Ashworth has four departments for which he is responsible: the first team; recruitment; the academy; medical and sports science.The logic is that if the manager goes, the new one is recruited into the existing framework — he does not bring in a whole new team. That ensures continuity and fosters a club culture. Ashworth is regarded as one of the best in the business at scouting players and compiling information on them, including background checks. He works well witht he manager and acts as a buffer between the manager and the chairman.

Ashworth was influential in brining many continental stars to the Hawthorns. People like Pablo Ibanez, the Spanish defender on a free contract, Gonzalo Jara for a pittance and Youssouf Mulumbu, a £75,000 DR Congo international that Paris St Germain didn't give a real chance. The list is also populated by players who were previously as anonymous as Ashworth himself, while even £4m on the likes of Peter Odemwingie and Somen Tchoyi hardly counts as lavish spending even at a club where the budget is notoriously tight.

His reputation has grown and helsea are believed to have noted Ashworth's work and included his name on their list of potential candidates to replace the departed Frank Arnesen as technical director at Stamford Bridge.

He was appointed Director of Elite Development for the English Football Association in September 2012 and took up the new role in March 2013. He is considered by many in the game to be at least partly responsible for England's significant upturn in results, particularly at age-group level and in women's football.

On 26th September 2018 it was announced that he had left his role with England to become Technical Director at Brighton.

He stood down from his role with Brighton in February 2022 and was placed on gardening leave until November 2022, under the terms of his contract. In May 2022 newspapers reported that Newcastle were considering paying some of the £5million that Brighton were demanding to release him. Ashworth's arrival at St James' Park would be the first major off-field appointment of the new Saudi-backed ownership, led in the UK by Amanda Staveley and her husband Mehrdad Ghodoussi. An agreement was finally reached on 30th May 2022 to formally release Ashworth from his contractual duties as Brighton & Hove Albion’s technical director and complete a move to the Magpies. Ashworth will be responsible for the club's overarching sporting strategy, football development and recruitment at all age levels, and will work closely with head coach Eddie Howe, academy manager Steve Harper and head of recruitment Steve Nickson.

In February 2024 Ashworth was put on gardening leave following an official approach by Manchester United. After Sir Jim Ratcliffe bought a 27% stake in Manchester United, he said on 21st February 2024 "I think Dan Ashworth is a 10/10 sporting director - one of the best around. He would be very good for Manchester United. It is understandable that somebody like Dan would see the Manchester United job as a very interesting challenge at this stage of his career. Ultimately, you can't really criticise Dan for looking at maybe the most coveted job in football as a sporting director - particularly with the challenge at Manchester United. What doesn't make sense is for Dan Ashworth to be sat doing nothing for 18 months."

On 1 July 2024, it was confirmed by Manchester United that Ashworth was appointed sporting director, following an agreement finalised with his former club, reported to be £3million. He lasted at Old Trafford until 8th December 2024. His Old Trafford exit was finalised in a meeting after the Red Devils' 3-2 home defeat by Nottingham Forest on Saturday, according to multiple sources with knowledge of the situation. A United statement said the decision was by "mutual agreement", adding: "We would like to thank Dan for his work and support during a transitional period for the club and wish him well for the future." United had had a disappointing season, sacking manager Erik ten Hag in October after just three wins from their opening nine Premier League matches. The club later confirmed it cost £10.4m to pay off Ten Hag and his staff, while the cost of paying a release clause to bring in his replacement Ruben Amorim was £11m. Owner Jim Ratcliffe commented that United had become mediocre and that difficult and unpleasant decisions would be needed.

In May 2025 Ashworth was appointed Chief Football Officer at the Football Association. He will lead high-performance strategy and the new-look St George’s Park.  The new role will have “strategic oversight across England men’s and women’s teams.,” The FA said, while he will also oversee regeneration of St George’s Park, which will undergo a significant upgrade to its facilities and pitches as England prepare to co-host Euro 2028.