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The club was founded in 1907 and in their early days competed in the North Berks League from the 1910–11 season. They left the North Berks league at the end of the 1927–28 campaign and later joined the Reading League and then the Metropolitan League. They then became founder members of the Hellenic League in 1953, where they won the championship at the first attempt. Although they returned to the Metropolitan League for the 1957–58 season they rejoined the Hellenic League Premier Division in 1963.

They spent the next thirteen seasons in the premier division before being relegated to Division one at the end of the 1975–76 season, the same season they made their debut in the FA Cup; however, they bounced back up as champions of Division one the next season. They moved between the Hellenic League's two divisions on two more occasions before they established themselves for the rest of their time in the top flight of the Hellenic league from the 1995–96 season. In 2004–05, under manager Stuart Peace, they were only denied the title due to the deduction of one point for fielding an ineligible player in a 1–1 draw at Tuffley Rovers at the start of the season, but made up for it by beating A.F.C. Sudbury to claim the FA Vase. The following season they finally claimed the league title, becoming the first team in Hellenic League history to accrue 100 points in a season, and were thus promoted to the Southern League Division One South & West.

In May 2009 they gained promotion to the Southern Football League Premier Division, when they beat AFC Totton 2–1 after extra time in the play-off final. Didcot reached the play-offs after finishing fifth in the league and, in consecutive matches, beating the first- (Truro City), second- (Windsor and Eton) and third-placed (AFC Totton) teams, all away from home. The 2010–11 season saw long-term manager Stuart Peace leave the club in January, to be replaced by Ady Williams; however, he could not save them from relegation.

Williams resigned in May 2011 to be replaced by Francis Vines, but he only stayed until September 2011, after a poor start to the season. He was replaced with Dave Mudge, who guided the club to the first round of the FA Trophy for the first time, but resigned at the start of the 2012–13 season for personal reasons to be replaced by Gary Elkins.

Elkins was replaced by former Didcot FA Vase winners Ian Concannon and Jamie Heapy, who were appointed as joint managers in November 2013 .

The football club gained nationwide attention when it reached the FA Cup first round proper in season 2015–16 and was awarded a home tie with Exeter City, which was shown live on BT Sport. At the end of the 2018–19 season, Didcot reappointed Jamie Heapy as their first team manager after Andy Ballard resigned.

The 2022–23 season saw Didcot Town promoted back to the Premier Division having defeated Ware in the play-off final.