At club level, Hamilton played for Linfield, QPR, Burnley, Oxford United, Limerick, Sligo Rovers, Coleraine and Distillery. He played in every game and subsequently scored two goals himself in the second round game against Austria, and also played at the 1986. Northern Ireland never lost when Hamilton scored.
In total, Hamilton played 41 games, scoring 5 goals, for his country.
He is also remembered fondly by Distillery fans. He was a sensational signing by the club as Player/Manager in December 1989, after leaving Limerick City of the League of Ireland, having managed them to a third-place finish in the previous season.
He made his playing debut for the Whites on 22 March 1990 and in his three seasons made 72 appearances and scored 33 goals including one hat-trick. Knee injuries forced him to end his playing career in February 1992, but he continued to manage the team up until February 1995.
He guided the club to the Gold Cup victory in the 1993/94 season.
Hamilton has the distinction of designing a board game, Billy Hamilton"s Football Academy, which was released in 1985. Scores and results list Northern Ireland"s goal tally first.