As a central defender, Hunter played for Coleraine (alongside his brother Victor), Oldham Athletic and Blackburn Rovers before making a £60,000 move to Ipswich Town, in a transfer that saw Bobby Bell heading to Blackburn. Despite interest from Everton and Leeds, Hunter chose Ipswich when he met Bobby Robson – "...within five minutes I had no doubt that Ipswich was where I wanted to go." Hunter spent the majority of his professional career with Ipswich, making over 350 appearances in his eleven years at the club, which included playing in the 1978 FA Cup Final in which Ipswich defeated Arsenal 1–0 at Wembley.