In his first full season, Johnson led his team to an automatic promotion to the Championship which earned him the division's Manager of the Year award.

After his playing career ended, Johnson spent the next six years training to earn his coaching badges and took his first managerial job at Newmarket Town in 1986.

However, once the decision was made to revert to being a part-time club, Johnson moved to Watford as director of their youth academy by request of former England manager Graham Taylor.

In his first year in charge at Huish Park, the Glovers won the FA Trophy by beating Stevenage 2–0 in the final at Villa Park as well as finishing third in the Football Conference; the following year they won the greater prize of the Conference championship by a record margin of seventeen points and topping the hundred goals mark too, winning promotion to the Football League.

In a show of good sportsmanship Gary Johnson told his players to allow Argyle to walk the ball into the net to level the score at 1–1, avoiding controversy.

Despite turning down an approach from Derby County in the summer of 2005, Johnson became Bristol City's target when their manager Brian Tinnion resigned that September.

After a 2006–07 season (including an 18 match unbeaten run), Johnson won the award again in March 2007 after successfully guiding his side to 16 points from seven games the previous month.

This had set Bristol City in a good spot to contend for automatic promotion, which they sealed on 5 May 2007 with a 3–1 home win over Rotherham on the last day of the season.

On 6 September 2007, Gary Johnson and assistant Keith Millen both signed 2+1⁄2-year contract extensions keeping them at the club until 2010.

[citation needed] In the summer before the 2008–09 season, he broke the club record for a transfer fee in signing 21-year-old Nicky Maynard from Crewe Alexandra for £2.25 million.

Under Johnson they had only managed to pick up six points, and it was only by beating Stevenage in the penultimate game of the season that they secured their survival.

[9] Northampton Town and Johnson parted company by mutual consent on 14 November, the team having secured just four wins in the new campaign.

Johnson was nominated for the January Manager of the Month award but missed out with Dean Smith of Walsall the eventual winner.

[citation needed] On 6 May 2013, Yeovil defeated Sheffield United 2–1 on aggregate to reach the League One play-off final.

[13] On 30 March 2015, Johnson was appointed as manager of League Two side Cheltenham Town, with the club bottom of the table two points from a position of safety.

[20][22] On 22 February 2024, Johnson left the club by mutual consent with them sitting 11th in the National League South.

[23] His departure came on the same day as Torquay United owner Clark Osborne announced plans to appoint administrators.