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Established in 1880, the club was initially closely linked to the Richard Garrett Engineering Works. They reached the final of the Suffolk Senior Cup in 1892, 1897 and 1904, losing on each occasion, although the club did win the Junior Cup in 1895. In 1894 Leiston joined the North Suffolk League, which they played in until 1909. In 1900 the club also joined the Ipswich & District League (later the Suffolk & Ipswich League) and were champions in their first three seasons. In 1904 they transferred to the South East Anglian League, but left in 1907 before rejoining in 1911 (when it had been renamed the East Anglian League). Between 1912 and 1914 the club also played in the Ipswich & District League.
After World War I the club was reformed as Leiston Works Athletic and rejoined the Ipswich & District League and the East Anglian League. In 1920 they left the EAL and joined the Essex & Suffolk Border League. At the end of the 1920–21 season the club left both the IDL and ESBL to join the Norfolk & Suffolk League before rejoining the IDL in 1926. After finishing bottom of the table in 1934–35 they were reformed as Leiston and dropped into Division 2B. The club won all seventeen league matches in 1937–38 and were promoted to Division One after defeating Division 2A winners Manningtree Rovers in a play-off.
In 1948 Leiston rejoined the Norfolk & Suffolk League, but transferred back to the Ipswich & District League in 1953. Despite finishing bottom of the Senior Division in 1979–80, the club avoided being relegated as the division was expanded. However, after finishing bottom again in 1981–82 they were relegated. They were promoted back to the Senior Division at the first attempt, also winning the Suffolk Junior Cup, which they retained in 1983–84. Leiston then spent several years as a yo yo club as they were relegated in 1988–89, promoted back in 1989–90, relegated again in 1991–92 and returned to the Senior Division in 1996–96. After finishing third in 2000–01 the club stepped up to Division One of the Eastern Counties League.
The 2003–04 season saw Leiston finish third in Division One, earning promotion to the Premier Division. The club reached the final of the Suffolk Premier Cup three times in succession between 2006 and 2008, but lost on each occasion; 3–2 after extra time against Lowestoft Town in 2006, 8–0 to Ipswich Town reserves in 2007, and on penalties to Needham Market in 2008. In the same season they beat Brentwood Town on penalties to win the East Anglian Cup. In the 2008–09 FA Cup the club reached the first round of the FA Cup for the first time; drawn at home to Conference North club Fleetwood Town, they drew 0–0 in front of a record crowd of 1,250, before losing the replay 2–0.
In 2010–11 Leiston won the Eastern Counties League Premier Division, earning promotion to Division One North of the Isthmian League. In 2011–12 they won Division One North, achieving back-to-back promotions and moving up to the Isthmian League Premier Division. They finished fifth in the Premier Division in 2017–18, going on to lose 1–0 in the play-off semi-finals to Dulwich Hamlet. The club were transferred to the Premier Central division of the Southern League at the end of the 2017–18 season as part of the restructuring of the non-League pyramid.