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Early history

Leighton Town F.C. was formed in 1885 and in their early years were winners of the Leighton and District League on several occasions. They were one of the original members of the South Midlands League (then known as the Bedfordshire County League) in 1922, the same year they changed their name to Leighton United (a change which lasted until 1963). They were also members of the Spartan League from 1922 to 1952, but their only successes were two Spartan League Division Two titles in 1923–24 and 1927–28.

In 1952, they became founder member of the Hellenic League but after two seasons moved back to the South Midlands League. In 1965–66, Leighton finished bottom of the Premier Division, but won the title the following season. They then returned to the Spartan League once again, followed by a two-year spell in the United Counties League before returning once again to the South Midlands League where they were to remain until 1992.

Promotion to Isthmian League

In the 1991–92 season Leighton won the South Midlands Premier Division title and stepped up to the Isthmian League, initially in Division Three, with promotion to Division Two following in 1996. The 2000–01 season brought relegation but the club bounced back in 2004, winning the title of what was now called Division Two. That same year re-organisation of the pyramid saw them switched to the Southern League.

Craig Wells resigned from the club early into the 2012–13 season – despite a strong end to the previous campaign, however he rejoined the side as manager in June 2013. Due to heavy debt and increasing costs the club made the decision not to pay their players for the 2013–14 season, becoming the only amateur side in the division.

Wells left the manager's position again in June 2014, replaced by former Ampthill Town boss Craig Bicknell.

After only one season at the club, Bicknell was sacked as the manager, despite the team reaching their best league position in recent years, and was replaced by former Arlesey Town, Hemel Hempstead Town, Aylesbury United and Aylesbury boss Mark Eaton in June 2015, Eaton was sacked at the end of October 2015 following a poor run of results, however a dispute between the departing manager and the club unfolded in the local paper.

Following Leighton Town's relegation from the Southern League Division One Central in 2016, the club parted company with manager Stuart Murray.

Return to Spartan South Midlands League

Murray was replaced by former Ashford Town (Middlesex) manager Paul Burgess in June 2016, as the club prepared for their first season back in the Spartan South Midlands Football League Premier Division following their relegation. Burgess resigned in November and was replaced with Scott Reynolds as interim manager, with Adam Kirkup and Lee Halling being appointed as his assistants, and Sean Downey continuing in his role as general manager. In May 2018, after a 4th placed finish in the league, manager Scott Reynolds resigned before being appointed as Aylesbury manager shortly afterwards. On 16 May, former Hemel Hempstead Town manager Danny Nicholls was appointed as his successor. However, in October 2018, Nicholls resigned after just 12 league games due to a poor run of form, with Aylesbury manager Reynolds also resigning just two days later. Joe Sweeney and Paul Copson were appointed as joint managers to replace Nicholls shortly after.