The original Ashton Town joined Division Two of the Lancashire Combination in 1903, and were promoted to Division One in their first season. However, they were relegated back to Division Two after finishing sixteenth in their first season in Division One. Towards the end of the 1910–11 season the club withdrew from the league and their fixtures were taken over by Tyldesley Albion.
The current club was established in 1953 as Makerfield Mill. They initially played in the Wigan Sunday School League, before moving to the St Helens Combination, in which they played for three years, winning Division Two in 1957–58. In 1958 they joined the Warrington & District League, winning Division One in 1959–60 and 1950–61. In 1962 the club were renamed Ashton Town after being forced out of their Windsor Road ground and moving home matches to a public park pitch at Whithill Street Recreation Ground in Bryn. However, they won the league again in 1962–63 and 1963–64.
In 1964 the club purchased their Edge Green Street ground, which had currently hosted Stubshaw Cross Rovers. They finished as Division One champions for a fifth time in 1964–65, before winning a sixth title in 1969–70. They subsequently joined the Lancashire Combination in 1971, moved to Division Two of the Cheshire County League in 1978 and became a founder member of Division Three the North West Counties League in 1982.
In 1985 the club dropped into Division One of the Manchester League, and despite only finishing sixth in the 1985–86 season, they returned to Division Three of the North West Counties League the following season. After Division Three was merged into Division Two in 1987, the club have remained at the same level since, with the division renamed Division One in 2008.