After leaving Arsenal, he made six appearances for Waltham Forest F.C., in the Ryman Division 1 North. He then joined the youth ranks at Cambridge United and after breaking into the first team he then moved to league club Northampton Town, where he signed on 16 May 2005. During his time at the club he was sent out on loan twice, playing for Gravesend & Northfleet and Stevenage Borough. Following the appointment of Stuart Gray as Northampton manager, Johnson featured in practically every single starting eleven that he named and he signed a new two-year contract extension.

Johnson began to attract attention from a host of Championship sides, including Coventry City, Colchester United and Queens Park Rangers, but was in talks to sign for Leicester City, after discussing terms at the Walkers Stadium on 2 January 2008. However, the player returned to the Sixfields Stadium, having failed to reach an agreement with the club.

Two days later, Leeds United confirmed reports that they had been given permission from Northampton to speak to Johnson, regarding a contract. He went on to sign a three-and-a-half-year deal for £250,000 after undergoing a medical at the club’s Thorp Arch training ground on 8 January 2008.

Johnson made his first appearance for Leeds on 14 January 2008 in their league fixture against Crewe Alexandra at the Alexandra Stadium. He scored his first goal for the club at Elland Road in a fixture against Bournemouth on 8 March. Johnson played for Leeds in the League 1 playoff final against Doncaster Rovers at Wembley, but was on the losing side as Leeds lost 1–0.

In November 2010, Johnson turned down the offer of a new three-year deal at Leeds United. Manager Simon Grayson initially confirmed Johnson had rejected a new contract but said that contract negotiations with Johnson would still be ongoing despite his refusal of the first contract offer. On 18 November, Johnson was transfer listed by Leeds after rejecting a final contract offer. Johnson was linked with Premiership clubs Bolton Wanderers and Stoke City.

On 13 January 2011, despite Johnson being on the transfer list, manager Simon Grayson said that he would not be able to sell Johnson unless a replacement had been brought in beforehand. On 18 January, Johnson scored his sixth goal of the season in an FA Cup Third Round Replay against Arsenal at Elland Road, a goal which later won Leeds’ goal of the season award.

Despite ongoing negotiations with Leeds, Johnson was unable to agree a new contract and on 1 July 2011 signed a three-year deal with Norwich City. He was handed squad number 4, which was vacated by Matthew Gill when he was released by the club. Johnson made his Norwich debut in the club’s first home match of the Premier League season. Johnson scored his first Norwich goal against Bolton Wanderers on 17 September 2011 at the Reebok Stadium with a “classy header”.

Johnson signed for Derby County for a club record £6 million on transfer deadline day on 1 September 2015. On 26 September 2015, he scored his first goal for the club in a 3–1 win over Milton Keynes Dons. On 26 November 2016, Johnson scored against his former club Norwich City – Derby won the match 1–0.

Johnson signed for Blackburn Rovers on a free transfer on 5 July 2019 after being released by Derby County. On 26 September 2020 he scored two goals against his former club in a 0-4 win at Pride Park.