The competition was originally known as the FAI Qualifying Cup before it was renamed the FAI Intermediate Cup at the start of the 1931–32 season. The cup's first winners were Drumcondra who beat Cobh Ramblers in the inaugural 1926–27 final. Drumcondra, who at the time were playing in the Leinster Senior League, subsequently went onto complete a cup double when they defeated Brideville 1–0 in the 1926–27 FAI Cup final.[2][3][4] The competition continues to act a qualifying competition for the FAI Cup with clubs who reach the Round of Sixteen being invited to compete in the senior cup.[1]
During the 2000s and 2010s Avondale United and Crumlin United have been the cup's most successful clubs. In 2013–14 Avondale United became only the second club after Distillery to win the cup four times in a row.[5][6] In 2012 the FAI introduced a new cup, the Tom Hand Memorial Cup, which saw the winners of the FAI Intermediate Cup play off against the winners of the FAI Junior Cup. Avondale United won the inaugural match, defeating Sheriff Y.C. 2–1 at the AUL Complex.[7][8]
In 2014 it was announced that future finals would be hosted at the Aviva Stadium.[9] The 2014–15 and 2015–16 finals were both played as double headers along with the FAI Junior Cup finals.[10][11]