Prior to becoming a manager, he played as a midfielder for Brighton & Hove Albion, Yeovil Town, Heart of Midlothian, Bristol City, Derby County, Chesterfield and Kilmarnock.

In February 2015 he took over as head coach of Barnsley, and a year later he was appointed as the new manager of Bristol City after an undisclosed compensation fee was agreed.

In 2000, Johnson signed for Brighton & Hove Albion, scoring in his only appearance for the club against Cardiff City in the Football League Trophy,[6] before having a non-contract spell with Brentford during the final months of the 2000–01 season, in which he failed to receive a call into the squad.

Johnson joined Scottish Premier League club Heart of Midlothian on 11 January 2006 for a transfer fee of £50,000, signing onto a two-and-a-half-year contract.

[5] His debut came as a late substitute in a 4–1 victory over Dunfermline Athletic,[9] and he started his first game in another 4–1 win over Hearts' Edinburgh derby rivals Hibernian.

[12] On 12 August 2006, Huddersfield Town manager Peter Jackson was sent to the stands after grabbing Johnson around the throat in a touchline incident 10 minutes from full-time.

On 10 February 2012, Johnson signed a two-and-a-half-year deal with Scottish side Kilmarnock, returning to Scotland after his departure from Hearts six years previously.

[14] On 18 March, he played in the Scottish League Cup final, in which Kilmarnock were victorious over Celtic, when Johnson set up the winning goal in their 1–0 success.

[25] Johnson made signings that would go on to make a big impact to Oldham's second half of the season, most notably the loan of Gary Harkins from St.

[30] During his first full season in charge, Johnson had Barnsley in mixed form prior to the new year period, picking up ten victories out of a possible thirty, including an eight-game losing streak.

[33] On 6 February 2016, Johnson was appointed as the new manager of relegation-threatened Championship club Bristol City, signing onto a three-and-a-half-year deal, after an undisclosed compensation fee was agreed between the Robins and Barnsley.

[33] Under Johnson's management, City went on to record several victories during their sixteen games in the league, eventually finishing a comfortable twelve points above the relegation zone in eighteenth place.

[38] Despite some fans demanding Johnson be dismissed, he remained as City manager ahead of the 2017–18 season, and brought in right-back Eros Pisano[39] and Senegalese striker Famara Diedhiou to boost their hopes of success, the latter signing for a club record transfer fee of £5.3 million.

[41] Later that month, as part of an interview for the BBC Points West programme, Johnson described his past of receiving death threats across the previous season, after completing the signing of Bristol Rovers striker Matty Taylor, also revealing how he was forced to move home, following the aftermath of his family's home address being publicised online.

On 14 March 2021, Sunderland won the 2021 EFL Trophy Final, beating Tranmere Rovers 1–0 courtesy of a goal from Lynden Gooch.

[54] Following a "rollercoaster" stint as Hibs manager, Johnson was sacked on 27 August 2023 after a third consecutive league defeat that left the club bottom of the Scottish Premiership.

"[59] After completing his tenure with CFG, he spent time with Danish Superliga club FC Copenhagen and also worked in Nigeria as a scout.