Later a central midfielder, Neil began his senior career as a callow, willowy young forward at Airdrie before joining Barnsley in 2000. He had broken through at impecunious part-timers Airdrie having been given a free transfer by Dunfermline the previous summer. Neil spent four years at Barnsley before joining Mansfield Town in 2004, where he spent only one season before signing for Hamilton Academical ("Accies"). Known for his aggressive playing style, he is a fan favourite for many of the Accies supporters. Neil won the Scottish First Division with the Accies in 2008 alongside James McCarthy and James McArthur. On 6 May 2011, Neil signed a new contract with Hamilton.
After manager Billy Reid vacated his managerial position at Hamilton in April 2013, Neil was appointed player/manager on an interim basis. He was made manager on a permanent basis on 24 May 2013, at the age of 31. Neil led the club to promotion back to the top flight in his first full season, winning through the play-off system in May 2014. Hamilton then enjoyed a good start to the 2014–15 Scottish Premiership, defeating Celtic away for the first time in 76 years.
In January 2015, Neil obtained permission from Hamilton to speak to Norwich City about their managerial vacancy. On 9 January 2015, Neil was confirmed as Norwich City manager at 33 years old. In his first game he managed his team to a 2–1 victory at Championship leaders AFC Bournemouth on 10 January 2015.