The club was formed on 28 April 2006 as a replacement for the town's previous club,
Runcorn F.C. Halton, which had resigned from the
Northern Premier League due to financial difficulties. The original Runcorn club's biggest success had been winning the
1981–82 Alliance Premier League title, although they failed to reach the
Football League as the league's members had voted against them joining. The club is run by the Supporters Trust, which had been set up as "The Linnets Independent Supporters Trust", and the new club joined two levels further down the
football pyramid, in the
North West Counties Football League Division Two, having been accepted into the league on 17 June. A groundshare with
Witton Albion was arranged at the start of the 2006–07 season, until a suitable ground could be found in Runcorn. This was achieved in 2010, when the club moved into a newly built ground on Murdishaw Avenue and named it the Millbank Linnets Stadium as part of a three-year sponsorship deal. Steve Carragher who had played for and managed Runcorn FC Halton, joined the club as manager, After three consecutive seasons of finishing runners-up, Runcorn finished fourth in the 2016–17 season, which was their lowest in four years. In the 2017–18 season, Runcorn Linnets finished the season in first, four points ahead of second placed
Widnes, who also gained promotion. Runcorn also went on to have the highest number of goals scored and the fewest goals conceded. After two seasons being cancelled due to the Covid pandemic, Runcorn finished 4th in the 2021–22 season. They beat
Leek 4–1 in the playoff semi final but lost 2–1 to
Marine in the playoff final with a sellout crowd of 1,600 at the APEC Taxis Stadium. Calum McIntyre left his role as manager at the end of season to join
Chester. In the 2022–23 season Runcorn made it to the
Liverpool Senior Cup final where they once again lost to
Marine on penalties at the
DCBL Stadium after a 0–0 draw in front of 2,651 fans. Runcorn finished 6th in this season with manager Dave Wild leaving the club before the play offs, with Billy Paynter taking over till the end of the season. The club went on to win away at
Leek in the playoff semi final before losing their third final in a year against
Workington 2–1 after extra time in the play off final, despite going 1–0 up early on. Billy then remained as Runcorn manager for the upcoming season. In the 2023–24 season Runcorn once again qualified for the Northern Premier League West playoffs with a second-place finish. They lost 2–0 to
City of Liverpool FC in the semi final. Following the loss, manager Billy Paynter stepped down from his position, after just over a year in charge.
Antony Kay was announced as the new Runcorn manager ahead of the 2024–25 season, after appearing 41 times for the Yellows the previous season. On 2 January 2026 after a 5-0 defeat at home to
Witton Albion FC, manager Brad Cooke stepped down and on January 5, Michael Ellison returned to the club as manager for a second stint after leading
Widnes FC to the title the previous year. ==Stadium==