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1920s

Athlone first competed in the League of Ireland in the 1922–23 season, finishing sixth. They were the first non-Dublin club in the Irish Free State to compete in the national Free State League. They competed in the league until 1928 and not again until the 1969–70 season.

Athlone Town won the FAI Cup, their first domestic success in 1924, beating Fordsons. Dinny Hannon scored the only goal of the game, as Athlone went through the whole competition without conceding a goal.

Hannon was one of five Athlone Town players chosen to represent the Irish Free State at the 1924 Paris Olympic Games. The other players were Tommy Muldoon, Frank Ghent, John Joe Dykes and Paddy O'Reilly.

Domestic success and European competition

The club finished second in the league in the 1974–75 season, earning a place in the UEFA Cup, the first time they had ever qualified for European competition. Their first-round game was against Norwegian side Vålerenga who they beat 3-1 at home before drawing 1-1 away. Athlone's second round tie was against Italian side AC Milan, drawing 0–0 in the first leg at St. Mel's Park, setting a record attendance of 9,000 before losing the second leg at the San Siro 3–0.

Athlone won their first league title in the 1980–81 season. They played KB in Europe the following season, earning a draw in the first leg in Denmark and again at St. Mel's Park, going out on the away goal rule.

In the 1981–82 season Athlone Town won the League Cup for the second time, beating Shamrock Rovers. However, they failed to retain their league title that year finishing 4th. Athlone Town were again crowned league champions in the 1982–83 season and qualifying for Europe, and also retained the League Cup, beating Dundalk. Their opponents in Europe on this occasion were Belgian outfit Raymond Goethals managed Standard Liège, losing 3–2 at home and 8–2 in Liège.

In 1985 six new clubs were elected to the league, increasing the league's participation to 22. As a result, the current two division (Premier and First) structure was adapted with Athlone Town in Premier Division. In 1987 the club finished last and were relegated to the First Division. Their stay there was short, finishing top of First Division the following season, gaining promotion to the Premier Division. The club remained in the top flight until the 1991–92 season, when they finished eleventh and were subsequently relegated to the First Division.

Athlone Town again gained promotion to the Premier Division in the 1993–94 season, finishing runners-up to Sligo Rovers that season.

Relegation

The club were once again relegated in 1996, narrowly missing out on promotion in 2001 by one point to Monaghan United.

Since 2001 Athlone have finished each season in the bottom half of the first division. In that time eight different managers have been appointed. In 2007 the club moved from St Mel's Park to a new stadium, which was opened on 9 March when the home side hosted Kilkenny City in the opening game of the season.

On 15 December 2008, the club held an emergency E.G.M. with supporters stating that they were in financial difficulties. Part finance had been raised and the club worked towards raising the rest. The club received funds through the patron scheme with over 350 fans contributing.

On 27 September 2013, Athlone clinched the First Division title with a 1–0 win over Waterford United.

In 2014, Athlone Town had a bad campaign in the Premier Division, finishing last in the championship, in the Leinster Senior Cup it was eliminated in the quarterfinals by St Patrick's Athletic, in the FAI Cup it was eliminated in the second round by Longford Town, and in the League Cup lost to Longford Town again in the first round.

In September 2017 the FAI banned goalkeeper Igors Labuts and midfielder Dragos Sfrijan for 12 months after a UEFA investigation found "clear and overwhelming betting evidence" of fixing of Athlone's 29 April match against Longford Town in the 2017 League of Ireland First Division. The Professional Footballers' Association of Ireland said the decision was based on "half-baked innuendo".

In 2018, a dispute over ownership of Athlone Town Stadium arose.

In November 2020, Athlone Town lost 11-0 to Dundalk F.C. in the FAI Cup semi final, a new record for the biggest win from a team in the history of the competition

There are many youth teams, ranging from u13 boys' to u17 women's team.

The club currently plays in the League of Ireland First Division.