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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, with Mark Philips as his assistant player-manager. Several players from the old club also joined the Linnets. Their first game was a 4–0 away win against Ashton Town, followed by a 5–0 victory at home to Castleton Gabriels. Runcorn finished their inaugural season as runners-up, losing out on the league title to Winsford United on goal difference, and won promotion to the First Division. Thomas Lamb finished the season as the top scorer, with 22 goals in all competitions.^[]

In the 2007–08 season, Linnets spent most of their time in mid-table. They won their first ever FA Vase game against Daisy Hill, before losing to Salford City in the First round. After a string of poor results, the board decided that a change of management was needed and Steve Wilkes was appointed as manager in January 2008. They finished the season twelfth out of 20 clubs. During the close season, the league was restructured with the First Division becoming the Premier Division. In the 2008–09 season Linnets entered the FA Cup for the first time, winning their first game 3–2 at home to Rossington Main on 17 August 2008. In the next round, they lost 4–0 to Curzon Ashton on 30 August. Recently the club has announced a youth team in every age group up to the under 16s. In 2011–12 they were the only team from the NWCFL to get to the Second Qualifying Round of the FA Cup.

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.

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 3rd final in a year against Workington 2-1 after extra time in the play off final, despite going 1-0 up early on.