After three years at Turf Moor he moved on to have a short spell at Notts County in 2010 and spent a season-and-a-half at cash-strapped Portsmouth.

He made 25[3] appearances in four years at Wimbledon and went out on loan to Brighton & Hove Albion to recapture his fitness following a serious cruciate knee-ligament injury.

While at the club he picked up three player of the season awards but had to finish his career in 1996 after another bad knee injury from which he was unable to fully recover.

He won the FA Trophy in 1998, beating Southport 1–0 in the final,[7] and Cheltenham finished second in the Conference the same year, their first season in that league.

[9] Cotterill took Cheltenham into the Second Division that season, following a play-off victory over Rushden & Diamonds at the Millennium Stadium in Cardiff.

[14] The side then went five matches unbeaten before Cotterill shocked the club on 10 October by handing in his resignation after just 13 games to become assistant manager to Howard Wilkinson at Sunderland.

[17] In February 2004, struggling Premiership outfit Leicester City appointed Coterill as coach by manager Micky Adams.

In 2005–06 he led Burnley to a 17th-place finish, again having to sell his star striker, the club's leading goal scorer Ade Akinbiyi to Sheffield United for £1.75 million.

[23] Cotterill eventually left the club on 8 November 2007 by mutual consent, after earning the title of longest serving manager in the league with three years seven months service.

[24] In August 2008, Steve Cotterill was offered the chance to become the head coach and technical director of USL First Division Minnesota Thunder after Amos Magee stepped down.

[36] On 4 October 2011, the joint owner of Portsmouth, Roman Dubov backed him saying "We support him and believe in him – his talent, his attitude and his work".

[37] It later became public knowledge that Nottingham Forest were interested in hiring Cotterill as their new manager after Steve McClaren resigned from his post on 2 October 2011 after 111 days in charge.

This followed the club's poor start to the season and allegations by McClaren of broken promises by the Nottingham Forest board regarding the signing of loan players.

[42] The turnaround was short-lived though as a run of seven games without a goal, during which Forest suffered six defeats leaving them in the bottom three at the turn of the year.

Forest ended that sequence with a 3–1 win at Ipswich Town on 2 January 2012[43] and followed that with a 0–0 draw at home to Leicester City in the third round of the FA Cup.

[45] From mid February, Forest's fortunes improved, starting with a 2–0 win over fellow relegation candidates Coventry City.

[49] In January 2013 he joined Queens Park Rangers to be part of Harry Redknapp's coaching staff on a short-term basis.

[56] Their form since the start of the season under Cotterill was described as "imperious" and promotion was gained on 14 April 2015 after a 0–6 away win at Bradford City.

[67] With three matches left of the 2016–17 season, Cotterill joined Birmingham City as first-team coach under new manager Harry Redknapp.

He played his part in preparing the team to gain the two wins needed to avoid relegation to League One, but decided against remaining with the club as assistant manager for 2017–18.

[70][71] After five months in post, during which the team remained in and around the relegation zone, and after a fifth successive league defeat – performance affected at least in part by a series of injuries and boardroom politics[72][73][74] – Cotterill was dismissed on 3 March 2018.

[75][76] On 27 November 2020, Cotterill was announced as manager of League One club Shrewsbury Town, just two days after the departure of Sam Ricketts.

[77][78] He took charge of his first game two days later, a 1–0 win at home to National League South side Oxford City in the second round of the FA Cup thanks to an extra time winner from Daniel Udoh.

[94] During 2021, Cotterill was twice admitted to Bristol Royal Infirmary with severe COVID-19 symptoms compounded by emphysema and a punctured lung.