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Founded in December 1942 as Annan Air Training Corps, the club changed their name to Annan Athletic the following April. They entered the Dumfries and District Youth League, but this competition lasted only throughout the war years, and in 1945 they joined the Dumfries and District Junior League instead. They had a fairly successful time as a junior club, reaching the fifth round of the Scottish Junior Cup on one occasion (losing 2–1 to Perth side Jeanfield Swifts).

In 1950–51 the Dumfries and District Junior League had to be wound up due to lack of officials, and the following season (1951–52) the club had to go into abeyance as the Junior Association would not release them from their membership. For the following season (1952–1953) Annan Athletic joined the Carlisle and District League and the Cumberland Football Association. This proved an astute move when Annan Athletic won every competition they entered bar one in their first season in membership.

Annan remained members of the Carlisle and District League until they moved back to Scottish football in the 1977–78 season when they joined the South of Scotland Football League. This switch, along with some upgrade work to their Galabank ground also allowed the club to compete in the qualifying stages of the Scottish Cup as well.

The club proved very successful in the South League, winning every competition that was available to them. In an attempt to get more competitive football, they joined the East of Scotland Football League in season 1987–88, although they maintained their commitment to the South League by running a reserve side. They won promotion in their first season in the East League, and two years later won the Premier Division. They became one of the league's top sides and qualified for the Scottish Cup's early rounds on various occasions.

Scottish Football League

Annan applied to join the Scottish Football League in 2000, when two new clubs were admitted, but lost out to Peterhead and Elgin City. Following the demise of local rivals Gretna in 2008, Annan applied along with four other clubs to replace them in the Third Division. They were the successful candidate, being chosen due to the standard of their facilities, ahead of Cove Rangers, Spartans, Preston Athletic and Edinburgh City.

Their first league match as a professional team ended in a 4–1 win over Cowdenbeath in the 2008–09 season. They finished 7th that season and 8th in the next season (however, they reached the semi-finals of the Scottish Challenge Cup). They were challenging for promotion to the Second Division in the 2010–11 season, their 3rd season in Scottish senior football. They finished 4th and qualified for the play-off final after a win over Alloa Athletic in play-off semi-finals (2–1, 0–0). They played Albion Rovers in the two-legged final, however, they lost the tie 4–3 on aggregate (1–3, 2–1), meaning that they missed out on promotion to the Second Division.

After the first quarter of the 2011–12 season, Annan sat top of the league, three points clear. Also, for the second time since becoming SFL members in 2008, they reached the semi-finals of the 2011–12 Scottish Challenge Cup. Later as the season progressed Annan dropped points and fell into mid table; they would then finish the season in 6th place, 8 points off the play-off places and 28 points off first position. A 3–0 defeat to First Division Falkirk ended their hopes of a first Challenge Cup Final.

During the 2012–13 season, Annan secured a 0–0 draw at home to Rangers on 15 September 2012, in what was the first-ever league meeting between the two sides. In the same season, on 9 March, Annan beat Rangers 2–1 at Ibrox, the first win for the club after the appointment of Jim Chapman as manager in January.

A second-place finish in the newly named SPFL League Two the following season included the clubs record points tally and saw them face Stirling Albion in the play-offs. After losing the first leg 3–1 the return leg at Galabank was an 8-goal thriller, Annan eventually losing 8–4 on aggregate.

In 2014–15 Annan produced an upset with a 3–2 win over Championship side Livingston in the Scottish Cup.

2015–2016 saw Annan miss out on the play-offs on goal difference as a final day 1–0 win over Queens Park proved not enough, the visitors pipping them to the spot by one goal. The season highlight once again came in the Scottish Cup after the first in what was to become a series of cup wins over Premiership side Hamilton Accies.

Forfar Athletic defeated Annan 6–4 on aggregate the following season in the play-offs, which signalled the end of Jim Chapmans reign.

Irishman Peter Murphy became only the third manager of Annan Athletic whilst an SPFL club, his first managerial role.

On 19 May 2023, they defeated Clyde 2–1 to earn a 5–2 aggregate play-off victory and seal promotion to Scottish League One, the club's first promotion to the third tier.