Flynn started his career with Burnley, and made his league debut for them in the 1973–74 season, when they were in the old First Division. After 120 league appearances he transferred to Leeds United in November 1977. He moved back to Burnley in November 1982 (after an earlier brief loan spell) and after 80 more league games Flynn moved to Cardiff City in November 1984.
Cusack's last game in charge on 18 September 2002 had seen Swansea lose 1-0 away to Boston United and move to last place in the Football League for the first time in their history. Flynn's first game on 21 September 2002 was no better for Swansea with them losing 1-0 at home to Torquay United. He set about trying to rebuild the side giving debuts to 21 players in his first season Their Football League status was only maintained on the last day of the season with them winning 4-2 at home to Hull City. The following season started well for Swansea and they made the FA Cup 5th round but after a loss of form, Flynn was replaced by Kenny Jackett.
Flynn joined the Welsh national set-up in 2004 as under-21 coach. His management of the Welsh under-21 side has seen some of the best results in its history. Flynn came agonisingly close to taking the Welsh team to the 2009 UEFA under-21 Championships, guiding the side to the top of a group containing France and Romania, including a superb away win against the latter. Unfortunately, competition rules stipulated that even group winners had to go through a two-legged play-off round in order to qualify, and Wales were knocked out 5–4 on aggregate against their neighbours, England.
Following the departure of John Toshack as Wales manager in September 2010, Flynn was appointed as Wales caretaker manager. He took charge of two games, both defeats. On 8 October 2010 Wales were beaten 1–0 in Cardiff by Bulgaria and on 12 October 2010 they lost 4–1 to Switzerland at St. Jakob-Park in Basel.
Having already been working for Doncaster Rovers as a scout, he was appointed as caretaker manager of the club on 7 January following Dean Saunders move to Wolverhampton Wanderers. At that point he was assisted by player Rob Jones who had been briefly installed as caretaker earlier that morning. On 17 January Flynn was confirmed as permanent manager with a contract till the end of the season. His first game in permanent charge of Doncaster on 19 January 2013 saw his side win 2–0 against Leyton Orient.
On 27 April 2013, Flynn secured promotion with Doncaster, and the League One title, with a 1–0 win against Brentford at Griffin Park. Victory for Brentford would have seen them promoted at Doncaster's expense, and they were awarded a penalty-kick in injury-time, but missed and Doncaster scored from the resulting counterattack to earn the victory.
At the end of the season, Flynn expressed a desire to step down as manager and return to a role of developing and recruiting players. Doncaster offered him a senior role in this as well as helping to choose the new manager. For the 2013−14 season he was named as Director of Football including overseeing the newly formed development squad which would be playing competitive games.