[6] 1937–38 saw the club achieve its best pre-war league position of runners-up,[2] before the competition was suspended due to the outbreak of World War II.

The Metropolitan League title was won for the second and final time in 1968–69 when the club reached the first round proper of the FA Cup for the first time in their history; 3,000 spectators saw the Blues hold Third Division leaders Bournemouth & Boscombe Athletic to a goalless home draw at King's Road, in a match covered by Anglia Television, but the replay at Dean Court was lost 3–0.

The 1970–71 season was the club's last in the Metropolitan League when they finished as runners-up and also lifted the Suffolk Premier Cup for the eighth occasion.

In 1986–87, which proved to be Bury Town's last season in the Eastern Counties League, the club enjoyed another good run in the FA Cup, reaching the fourth qualifying round.

Bury saw little success until the 2004–05 season with the club finishing second in the league and winning the Westwood Shield, as well as reaching the quarter-finals of the FA Vase for the second time.

In the same season they reached the first round proper of the FA Cup for the first time in forty years, losing 4–2 away to Conference North club Alfreton Town.

The following season they won the Premier Cup for a tenth time, defeating Needham Market 2–0 in the final, and also finished third in the league, qualifying for the play-offs, where they lost 2–1 at home to Lowestoft Town.

[2] It became the first football ground in East Anglia to operate floodlights, when on 12 January 1953, Bury played their first ever floodlit game against Cambridge City in front of 2,105 spectators.

[11] Note: Flags indicate national team as defined under FIFA eligibility rules; some limited exceptions apply.