The club are members of the Cheshire Football League, and as from season 2016–17 play their home matches at Ruskin Drive Sports Ground, which they share with local rivals Pilkington.

They took out a lease on the former cricket ground at Hoghton Road, Sutton, adjacent to the St Helens Junction railway station and, although the club entered the FA Cup in the 1946–47 season, a team could not be raised in time to fulfill the tie with Prescot Cables.

An all-time club record attendance "between 8,000 and 9,000" witnessed a friendly game against Manchester City which was arranged as part of the Trautmann transfer deal in April 1950.

Following a second relegation in 1956, St Helens Town continued to play in the Lancashire Combination, winning the Championship in 1971–72, by nine points ahead of Accrington Stanley.

But they obtained ample compensation by winning the FA Vase in 1987, beating near neighbours Warrington Town in the final 3–2 with a Phil Layhe brace and a goal from Brian Rigby.

[1] They were regular promotion candidates for many years, largely due to the goalscoring exploits of Steve "Pellet" Pennington, who grabbed 216 goals, his season's best hauls of 45 in 1993–94 and 46 in 1997–98 just fell short of the club record of 47 scored by Phil Stainton in 1963–64.

Town, having gone into partnership with St Helens R.F.C., ground-shared Knowsley Road for 10 years, but the intended relocation to the new Langtree Park ground did not materialise.

The goalkeeper played a single season with the non-league outfit, including in front of a record 9,000 attendance in the final of the local Mahon Cup,[3] before moving on to Manchester City in 1949.