Having spent over four years on the coaching staff at Rochdale, Flitcroft followed manager Keith Hill to Barnsley in June 2011 and was appointed caretaker-manager following Hill's sacking in December 2012. He was given the job on a permanent basis and kept the club in the Championship at the end of the 2012–13 season, only to be sacked in November 2013. He was appointed as Bury manager the following month and quickly found success, being named as Manager of the Month for February 2014. He led the club to promotion out of League Two at the end of the 2014–15 season and kept the club in League One the following season. Despite being named as Manager of the Month for September 2016, he was sacked two months later following a poor run of form. He took charge at Swindon Town in June 2017, before changing clubs to manage divisional rivals Mansfield Town in March 2018. He was sacked in May 2019 after the club were beaten in the League Two play-off semi-finals. Keith Hill named him as his assistant at Bolton Wanderers in August 2019, though the pair were not retained beyond the 2019–20 season. He was appointed director of football at Port Vale in February 2021.
