Paul only had a brief spell at Carrow Road; joining the Canaries from Wigan in May 1988 for £73,000 and leaving for Wolverhampton Wanderers in December 1989. Faced with competition with Ruel Fox and Jeremy Goss on the right side of the Norwich midfield, Paul was limited to just eight appearances, four of which were as substitute.
After approximately 200 games for Wolves, Paul moved to the top flight with Coventry City. 37 appearances followed before a move down one division with Tranmere Rovers in March 1996 for £250,000. In October 1997 he joined Gary Megson's Stockport County for £250,000 and scored on his debut.
Paul joined Burnley on loan on 25th March 1999. Impressing in his 12 games for the Clarets, Cook eventually signed for Burnley in early July 1999 on a free transfer. By the end of the 2000/01 season, Paul had made 96 league appearances for Burnley scoring 7 goals. Paul spent December 2001 on loan to Wigan Athletic.
Returning to Burnley, Paul made many more appearances to take his total to almost 200 games. Out of contract at the end of the 2002/03 season, he announced in April 2003 his retirement from the professional game. He was persuaded otherwise by Accrington Stanley preparing for their first season in the Conference who signed him in late May 2003 Paul is now primarily working as a coach for Stanley and was part of their management team that led them to promotion to the Football League in April 2006 after 44 years away.
In June 2006, he was appointed as Southport's first ever full-time manager, replacing Liam Watson. He lasted in this role until 3rd January 2007, departing the club after a run of three straight defeats over Christmas 2006 left them bottom of the Conference. Cook's Southport had managed just four wins in the first half of the season.
Paul Cook was named as the new Sligo Rovers manager on April 27th 2007, taking over from Rob McDonald. He guided Sligo to a credible 6th place league finish in his first season. At the end of his second year (2008) he guided Sligo to fourth in the league and thus secured a UEFA Cup place.He departed in January 2009 by mutual consent but was re-appointed a few weeks later.
In his third season, under sever financial constraints, he guided Sligo to sixth place. In addition, Cook guided Sligo to the final of the FAI Cup which took place on the 22nd November 2009. Sligo lost 2-1 to Sporting Fingal despite holding a one goal lead with seven minutes remaining. His first silverware as Sligo manager came in September 2010, after a 1-0 win over Monaghan United in the final of the League Cup. In November 2010, he guided Sligo Rovers to win the 2010 FAI Cup Final, 2-0 in a penalty shoot-out against Shamrock Rovers
With successes like these, he was linked in January 2011 to the managerial vacancies at former clubs Burnley (along with Paul Lambert and Malky Mackay) and Stockport
He was also linked in October 2011 with the managerial vacancy at Scottish Premier League side St Johnstone but they could not agree terms. Steve Lomas was eventually appointed St JOhnstone's manager.
In February 2012, Paul returned to England to manage his former club Accrington Stanley.
On 25th October 2012, Paul quit Stanley to become manager of rivals Chesterfield. He led them to the League Two title in 2013/14.
In May 2015, Paul quit to take charge of Portsmouth (in League Two) despite taking Chesterfield to the League One play-offs (where they lost to Preston in the semi-final).
On 17th April 2017, Portsmouth secured promotion to League One with a 3-1 victory over Notts County. They beat Cheltenham 6-1 on the closing day of the season to secure the League Two title. Cook was then linked on 13th May 2017 by BBC Radio Solent with a return to his former club Wigan who had just been releaged to League One. This was completed on 31st May 2017 with Cook signing a three year deal and Wigan paying compensation to Portsmouth. Cook said ""It was only a minute ago at Portsmouth we were winning the league and we really did think our future was going to be there. But the way things have transpired with new ownership coming in that isn't the case,"
In his first season at Wigan, he led them to the League One title which was secured on 5th May 2018. The 1-0 win at Doncaster gave them 98 points.
In July 2020, following Wigan's decision to enter administration, Cook was linked with the managerial vacancies at both Bristol City and Birmingham City. However his Wigan side were not willing to accept the 12 point deduction meant relegation and thrashed Hull City 8-0 - a Championship record victory. Cook resigned from Wigan on 1st August 2020 "with a heavy heart" Wigan, who won 10 of their last 18 games in 2019-20, were relegated on 22 July after a 12-point deduction for entering administrationWigan later lost their appeal.
Paul Stanley, on behalf of the joint administrators, added: "Throughout the past few weeks Paul has been an admirable leader for the football club. We have been inspired by the way he has worked with his staff and the players to produce an incredible run of results and performances. We have had an open and transparent relationship with Paul during our few weeks of involvement with Wigan Athletic and we have appreciated his integrity from day one. On that basis, we felt it was important we allowed Paul to leave his role as manager." Paul was linked with the managerial vacancy at Bristol City. He was linked again with the Bristol City vacancy in February 2021
He was appointed as manager of Ipswich Town on 2nd February 2021 signing a contract until the summer of 2023. He was sacked on 4th December 2021 after winning just 13 of his 44 games at the helm. The final straw was the goalless FA Cup home draw with League Two Barrow. Ipswich chief executive Mark Ashton said: "Following discussions with the board, we have decided a change is needed for our long-term interests.I know how much Paul wanted to succeed at this club. At this moment, there is no one lined up to replace him.
On 7th February 2022 BBC Radio Sheffield reported that Cook was in talks with Chesterfield regarding a return as manager as a replacement for the departed James Rowe. This was confirmed on 10th February 2022. Chesterfield chief executive John Croot said "We are delighted to welcome Paul back to the club. He enjoyed great success here previously and to secure someone with his impressive track record is a real coup. Paul was our number one target when we began our search for a new manager and we are sure that our supporters will share our delight that he has agreed to take the role."
On 20th December 2023 Cook was linked with the managerial vacancy at Plymouth caused by Steven Schumacher's decision to switch to Stoke as replacement for Alex Neil. Cook's profile was high with Chesterfield riding high at the top of the National League.