The cup's first winners were Drumcondra who beat Cobh Ramblers in the inaugural 1926–27 final.

[1] In addition to being the inaugural winners, Drumcondra were also the first of several future League of Ireland clubs to win the FAI Intermediate Cup.

Cork Bohemians, Sligo Rovers, Longford Town, UCD, Cobh Ramblers, St Patricks Athletic, Albert Rovers, Bray Wanderers, Home Farm and Cork Hibernians, playing as AOH, all subsequently won the cup before joining the national league.

Jacobs, St. James's Gate and Transport all won the cup after leaving the League of Ireland.

The reserve teams of League of Ireland clubs have also won the cup on several occasions.