The club was founded in 1889, but the exact date is not clear. The club's first appearance in the Kerry Senior Football Championship was the following year. In 1891, Milltown entered two teams. It was the only club to do so. This was a great feat as both teams were composed of 21 players. They had some success with the A team, the Milltown Volunteers, winning a few games, only to be beaten by Laune Rangers. In 1892 the club entered one team. It won the first two games beating Cordal and Tough, only to be defeated by Ballymacelligott. Milltown club then seems to have declined for a few years as it didn't contest the County Championship again until 1900.
After 1913, Milltown GAA Club no longer appears to have contested the County Football Championship. In 1947 Milltown won the Mid Kerry Senior Football Championship. Early in the 1950s it amalgamated with Castlemaine and as Milltown-Castlemaine won this championship in 1953,1955,1957, 1961,1962,1972, 1989, 2001, 2007,2008 and most recently in 2010
They also won the Kerry Novice Football Championship in 1979 and the Kerry Junior Football Championship in 1990. Milltown/Castlemaine won the Kerry Intermediate Football Championship in 1991, 1994 and again in 2003.
In 2001 the club had an historic year, winning the Kerry County Football League - Division 1 title and also the Mid-Kerry Championship. 2004 was a special year for the club when they won the Kerry Club Championship.
The club won the All Ireland Intermediate championship in 2012 by beating Davitts of Mayo in the final.