In October 2016, the club's senior side suffered relegation from the Premier Division at the end of a very disappointing 2016 season. Previously 'the Town' was promoted to the Premier Division at the end of the 2014 season following a seven-year stint in the First Division.
Longford Town was founded in 1924 but had to wait 60 years for election to the League of Ireland in 1984. In their first season in the league they finished last in the Premier Division and were one of the four sides to be relegated to the newly created First Division for the following season. In their second season they finished bottom of the First Division with only 7 points. They finished in the bottom six of the ten team First Division in each of the next eleven seasons. In the 1998–99 season they missed out a place in the promotion/relegation playoff by just four points. The following season saw a further improvement when they finished 2nd in the First Division and as a result won promotion to the Premier Division. Longford had a decent season in the Premier Division in 2000–01 finishing in mid-table. That season also saw the club reach the FAI Cup final for the first time where they lost 1–0 to Bohemian. As Bohemian also won the League title that season, Longford Town FC qualified to play in the UEFA Cup in July 2001. A meeting over 2 games with Bulgarian club side PFC Litex Lovech ended in a 3–1 aggregate victory for the Bulgarians.
Things were less comfortable in the league during the 2001–02 season after that as they ended up in the relegation/promotion playoff. They had to play Finn Harps and they survived in Premier Division just about. They won in a penalty shootout after the tie ended 3–3 on aggregate. After that tough season the club became an established top division team with four successive top six finishes in the four seasons immediately after that. They also reached three more FAI Cup finals winning two of them. In 2004 they produced a cup double by winning the League of Ireland Cup in addition to retaining the FAI Cup. Because of their back-to-back FAI Cup successes the club entered European competition for two seasons in a row. On both occasions, however, they lost in their opening tie. In 2006 Longford finished in 8th place in the league. The 2007 season was a disappointing one for the midlands club as they finished last in the division and as a result were relegated. That is not the whole story, though, as the club were deducted six points during the season for failing to comply with club licensing procedures. These six points proved crucial in the end, as without this deduction they would have finished safe from relegation and the relegation play-off. This cost the club dearly, as there followed six frustrating years in the First Division, before being promoted as champions at the end of the 2014 season. The title was clinched following a resounding 5–0 victory at home to Shamrock Rovers B on October 3, 2014.  In their first season back in the Premier Division, the Town finished off the 2015 season in 6th position. The 2016 league season was very disappointing with Longford finishing bottom and relegated back to the First Division.