In May 2009, Rowett was named as assistant to newly appointed manager Paul Peschisolido at Burton Albion. Rowett was put in temporary charge of Burton, assisted by Kevin Poole, following Peschisolido's sacking in March 2012. On 10 May, Rowett was announced as the permanent manager of Burton Albion. In his first season, he led Burton to fourth place in League Two, losing in the play-off semi-final to Bradford City, and followed up with a sixth-place finish in 2013–14 and a 1–0 defeat to Fleetwood in the play-off final.
In September 2014, with Burton near the top of League Two, Rowett rejected the opportunity to manage Championship strugglers Blackpool; he said he felt it was not the right job for him at the present time. On 27 October, he was appointed manager of his former club, Birmingham City – one place above Blackpool at the bottom of the Championship table. He was joined at Birmingham by Burton backroom staff members Kevin Summerfield as assistant manager, Mark Sale as first-team coach and Poole as goalkeeping coach. All three are also former Birmingham City players. Rowett guided Blues from 21st in the championship to 10th at the end of his first season, earning many plaudits for the remarkable turnaround in form.