The club have spent 34 seasons in Scotland's top division altogether, though the last was in the 1977–78 season. The club have been the champions of the second tier of Scottish football on six occasions and of the third tier twice, but have not won any national cup competitions. The club's most famous and most successful manager is Ally MacLeod, who went on to manage the Scottish national football team. On 15 May 2012, it was announced that Mark Roberts would succeed Brian Reid as manager of the club, following relegation to the Second Division at the end of the 2011–12 season In January 2015, Ian McCall was appointed as Ayr's new manager, taking over from Roberts.
Ayr United were founded in 1910 after the merger of Ayr Parkhouse and Ayr. Although Inverness Caledonian Thistle are also the product of a merger between two clubs, Ayr United are the only Scottish Football League club to have been formed from a merger of two existing league clubs.
The club's honours include winning six Second Division titles (as the second tier championship) and a further two such titles (as the third tier championship), most recently in 1996–97. They have not won any national cup competitions, although they were runners-up in the 2001–02 Scottish League Cup, and in the Scottish Challenge Cup in the first two seasons in which the competition was held: 1990–91 and 1991–92. They have won the local competition the Ayrshire Cup on 26 occasions, most commonly facing fierce local rivals Kilmarnock F.C. in the final. The Ayrshire Cup was last played for in season 1996–97, since when the competition has been suspended.
The club's record scorer in a single season is Jimmy Smith, who scored 66 goals for Ayr in only 38 league matches in 1927–28, which puts him second in the British goalscoring record for a single season (after Fred Roberts, who scored 96 goals for Glentoran in one season in 1930/31). The club's overall record scorer is Peter Price, who scored 213 times in competitive matches for the club between 1955 and 1962.
Former Scottish national team manager Ally MacLeod is regarded as the club's most famous and most successful manager. He led the club on three separate occasions spanning fifteen years, during which his teams recorded a record 214 wins, won two league titles and finished one point short of qualifying for European competition in 1973, when Macleod was also voted as Ayr's Citizen of the Year. More recent managers have also included the recent Scottish national team manager, George Burley, and former Scottish League Cup winner with Raith Rovers, Gordon Dalziel. Their current manager is Mark Roberts.
Although the club has spent 34 seasons in Scotland's top division, they have played in the second and third tiers of Scottish senior football since the 1977–78 season. During the late 1990s and early 2000s, the club established a record of defeating teams which played in higher leagues in cup competitions, including Hibernian, Dundee, Dundee United, Motherwell, Dunfermline Athletic and four consecutive wins in cup competitions against their fiercest rivals Kilmarnock.
In 1988, Ayr United fan and businessman Sir David Murray offered to buy the club but the club's shareholders rejected the bid by a vote of 60 to 56. The manager at that time, Ally MacLeod, had threatened to leave if Murray's bid had succeeded: Murray went on to become Chairman of Rangers, which coincided with a period of financial growth and league success for that club. During much of the 1990s and 2000s, a period of relative success both in league and cup competitions, the Ayr United chairman was local construction magnate Bill Barr. After Barr stood down, there were occasional boardroom struggles: the club suffered significant cashflow problems in 2004 although it survived with a combination of efforts. Prestwick-based Roy Kennedy failed to takeover the club in 2005, and his company Kennedy Construction went bankrupt in 2006.
On 24 May 2009, Ayr won the Scottish First Division Play-off against Airdrie United 3–2 on aggregate to win promotion to the First Division. For season 2009–10, to celebrate the club's centenary, Ayr United played in black and white hoops, the club's original black and white kit. The away kit was crimson and gold with blue shorts to reflect the original club colours. Ayr were relegated on the last day of the season after losing 2–1 to Morton. At the end of the 2010–11 season, Ayr United defeated Forfar Athletic 7–4 on aggregate in the First Division play-off semi final, to set up a final with Brechin City. In the first game at Somerset Park the match ended 1–1, however Ayr United won the second leg at Glebe Park 2–1, which promoted Ayr United to the First Division for the 2011–2012 season. Also, in the 2010–11 season, they knocked out Hibernian in the Scottish Cup, winning 1–0 at Somerset Park in a replay.
On 15 May 2012, Ayr United announced that Brian Reid's contract would not be renewed, with the club appointing Mark Roberts, top-scorer in the previous three seasons, as manager, with head of youth development, Davie White as his assistant.
The club's original jerseys were red and gold, inherited from Ayr FC, with navy blue shorts and socks. In 1914, Ayr adopted black and white hoops, which were worn, with several modifications, up to 1930, when The Honest Men switched to a plain white jersey, with navy blue shorts and socks, worn until the outbreak of World War II. After the war, the club retained the white jersey, and switched back to the black shorts that had originally complimented the hooped shirts, kits similar to these were worn up to 1958, when Ayr had changed the black and white look for a white with a blue trim, used until 1963, when they once again reverted to the black and white hoops, that were kept until 1968 and not used again until the 2009–10 centenary season. From then until 1994, Ayr maintained white jerseys trimmed with black with either black or white shorts and socks, then switching to a striped shirt for a single season. The following season, Ayr wore an all-black jersey for the first and only time. Ayr went back to keeping an all-white jersey with either white or black shorts and socks until the centenary season. For the 2011–12 season, a half-black-half-white shirt for the first time, however, Ayr FC had previously wore a similar jersey between 1899 and 1903. The 2013–14 season saw Ayr return to the white jersey, black shorts and socks for the first time since 1973.
Ayr play their football at Somerset Park in Ayr's New Town. One of the few surviving traditional stadium designs, it consists of one stand, two covered terraces, and one open terrace. It has a capacity of 10,185. The first match to take place at Somerset Park was between the former Ayr F.C. and Aston Villa in a 3–0 victory for Ayr.
During the 1990s the club's chairman was Bill Barr, who owned and managed the company which built modern-style stadiums and stands for several other clubs around the UK. United also sought — and obtained — planning permission from South Ayrshire Council for a new 10,200 all-seated stadium at Heathfield in Ayr with an associated retail development. The Scottish Executive then "called in" the application and reversed the decision in respect of the retail development. Since the club considered this aspect of the proposal necessary to fund the construction, the development did not proceed.
In November 2006, United signed a contract with Barratt Homes for the sale of Somerset Park, having secured a 20-acre (81,000 m2) site in the Heathfield area of Ayr. The site would house a new £18 million stadium seating 7,650 as part of a "sports and business campus". The project did not ultimately proceed.