Flitcroft began his footballing days with Preston North End. After four years at Deepdale and a brief loan spell at Lincoln City, the midfielder moved to Chester City where he amassed more than 200 first-team appearances.
In 1999 he moved to Rochdale, helping the Dale to the Division Three play-offs in 2002 before his four-year stay at Spotland came to end - joining Macclesfield Town for six months. He later moved back to Lancashire, signing for Bury where he made a century of appearances as a stalwart in the middle of the park. Overall in the Football League he made over 500 appearances for Preston, Chester, Rochdale, Macclesfield and Bury.
Midway through the 2006/07 season, Flitcroft teamed up with Keith Hill at Rochdale - becoming Hill's assistant.
The management duo were highly regarded during their time at Spotland, after guiding the Dale out of League Two via the play-offs and then to their highest ever position in forty years - ninth in League One, at the end of the 2009/10 campaign.
His first managerial appointment at Barnsley followed a brief spell as caretaker manager and prior to that he was assistant manager to Keith Hill at Oakwell from June 2011. After taking charge, Flitcroft went onto secure the club's Championship status.
He later joined Bury in the 2013/14 season and guided the Club to a 12th place finish in Sky Bet League Two.
In the 2014/15 season Bury acheived promotion to League One, completing the season in 3rd place.
Flitcroft was appointed as manager of Swindon Town on the 5th June 2017.