Luton Town Football Club was formed on 11 April 1885 after a series of meetings and discussions among prominent clubs in the town. The idea of forming a 'Town' club to include the best players in Luton was proposed by George Deacon and eventually led to the establishment of Luton Town Football Club.

In 1890, Luton Town started making payments to individual players, marking a significant shift towards professionalism in the club. This move paved the way for Luton to become the first fully professional club in southern England the following year.

In 1894, Luton Town F.C. was one of the founding members of the Southern League.

In 1897, Luton Town F.C. became a member of the Football League, playing for three seasons before leaving due to financial struggles.

Luton suffered their heaviest loss with a 0-9 defeat against Small Heath in the Second Division on 12 November 1898.

Due to financial challenges and high costs associated with competing in the Football League, Luton Town made the decision to return to the Southern League for the 1900–01 season. This strategic move aimed to ensure the club's sustainability and competitive edge.

After the sale of their Dunstable Road ground for housing in 1905, Luton Town had to move to their present Kenilworth Road site at short notice, in time for the start of the 1905-06 season.

Left winger Robert Hawkes became the first player to be capped while playing for Luton when he represented England against Ireland at Goodison Park on 16 February 1907.

On 21 November 1914, Luton achieved their largest win with a 15-0 victory over Great Yarmouth Town in the FA Cup.

In 1920, Luton Town F.C. returned to the Football League, which had expanded to include a third tier by that time.

During a match between Ireland and England in 1921, three Luton players, Louis Bookman, Allan Mathieson, and Ernie Simms, showcased their talent on the international stage, highlighting the club's strong presence in football.

In 1933, Luton Town Football Club adopted a badge depicting a straw boater, which appeared on the team's shirts, marking a significant change in the club's crest.

Joe Payne set the Football League record for the most goals in a game by scoring 10 goals against Bristol Rovers on 13 April 1936.

Joe Payne scored twice in his only game for England against Finland on 20 May 1937, becoming the first player to score in an international match while at Luton.

Luton's highest home attendance of 30,069 was recorded during a match against Blackpool in the FA Cup on 4 March 1959.

In 1965, Luton Town FC slumped to Division Four amidst apathy and dwindling crowds, only six years after their FA Cup Final appearance. The club faced significant challenges during this period.

After going to the top of the table in February 1968, Luton Town F.C. never looked back and walked away with the title, piecing together a squad that included a mix of youth and experience.

The collapse of Burr and Hunt's Vehicle and General in March 1970 had a disastrous impact on Luton Town F.C., leading to a halt in their meteoric rise and making the club sellers rather than buyers.

In 1971, Luton Town F.C. sold their proven goalscorer, Malcolm Macdonald, to Newcastle for a then massive £180,000, resulting in a complete anti-climax for the club in the following season.

In 1973, Luton Town introduced a new badge featuring a stylised orange football with the letters 'Lt' and the club's name in navy blue text, coinciding with the switch to an orange kit.

In 1974, Luton Town released the song 'Hatters, Hatters', a collaboration between the team and the Barron Knights musical comedy group.

Starting in 1979, Luton Town Football Club began playing in white shirts, shorts, and socks, with the orange and navy motif reduced to trim on the kits.

Tricentrol, a local motor company based in Dunstable, became the first sponsor on a Luton Town shirt from 1980 to 1982, with a deal worth £50,000.

On the last day of the 1982–83 season, Luton Town, playing against Manchester City, needed to win to avoid relegation. A late winner by Yugoslavian substitute Raddy Antić saved the team, leading to manager Pleat dancing across the pitch in joy.

In 1984, Luton Town F.C. achieved victory in the Football League Cup.

In 1986, Luton Town introduced executive boxes at Kenilworth Road Stadium, replacing the Bobbers Stand, as part of the club's efforts to maximize income.

In 1987, Luton Town switched back to a badge derived from the town emblem, with the shield portion of the heraldic crest becoming the team's badge, retaining the club name in navy blue.

On 24th April 1988, Luton Town won their first ever major trophy, the Littlewoods Cup, with a last-minute 3-2 victory over Arsenal at Wembley. The thrilling match saw Brian Stein scoring the winning goal after Andy Dibble's brilliant penalty save.

In 1989, Ray Harford was dismissed as the manager of Luton Town mid-way through the season after a last gasp win over Norwich. Jim Ryan, a former Hatters star, took over but could only help the team escape relegation over the next two seasons.

From 1990 to 1991, Luton Town had Vauxhall as their shirt sponsor.

In 1992, after 10 years at the top level, Luton Town were relegated to Division Two. The team struggled to adapt to the new level and almost faced another relegation in 1993.

The 'rainbow' badge was introduced in 1994, featuring the town crest, an orange and blue bow, two footballs, and the club name in navy blue text, which was used until 2005.

From 1999 to 2003, SKF sponsored Luton Town's shirts.

The team had a challenging season in the 2nd Division in 2000-01.

In the 2001-02 season, the team achieved success in the 3rd Division.

The team performed well in the 2nd Division during the 2002-03 season.

The team achieved promotion to the 2nd Division in the 2003-04 season.

In the 2004/05 season, under manager Mike Newell, Luton Town won the League One title with a fantastic start, winning their first six games and finishing 12 points clear of nearest rivals Hull City.

Under manager Mike Newell, Luton Town finished as champions of the rebranded third-tier Football League One in the 2004–05 season.

Luton Town was relegated twice in a row, starting in the 2006-07 season. The team faced financial difficulties and struggled to maintain their position in the league.

Luton Town spent the latter part of the 2007-08 season in administration, leading to a ten-point deduction from that season's total. The club faced challenges both on and off the field.

Luton Town confirmed their relegation to League 2 after a 2-1 home defeat to Brighton on April 12, 2008. The team struggled to find form and young players were low on confidence.

Luton Town came from behind in the final of the Football League Trophy to win the competition for the first time. It was a significant achievement for the club after facing various challenges.

In the 2012–13 FA Cup fourth round, Luton Town secured a historic 1-0 victory over Premier League club Norwich City, becoming the first non-League team to defeat a top division side since 1989.

Luton Town had a successful run in the 2012/13 FA Cup, beating teams like Wolves and making history by becoming the first non-league side to beat a Premier League team, Norwich City.

Under the management of John Still in the 2013–14 season, Luton Town clinched the Conference Premier title with three games remaining, earning a promotion back to the Football League from 2014–15.

In 2015 to 2016, Barnfield College and NICEIC sponsored Luton Town's shirts.

Connor Tomlinson became the youngest player to make a first-team appearance for Luton Town at 15 years and 199 days old in the EFL Trophy match against Gillingham on 30 August 2016.

Luton-born full-back James Justin was transferred to Leicester City on 28 June 2019 for the highest fee received by Luton Town for a player.

Luton Town competed in the first round of the English Football League Cup in the 2020-2021 season. James Collins scored 3 goals and James Shea had a notable performance in the match.

Luton Town participated in the third round of the English FA Cup during the 2021-2022 season. Reece Burke scored 2 goals and Jed Steer also played a significant role in the match.

Luton Town played in the first round of the English Football League Cup in the 2021-2022 season. Admiral Muskwe and Cameron Jerome scored 1 goal each, with James Shea also contributing to the match.

The management team of Luton Town as of October 2021 includes Chief Recruitment Officer Mick Harford, Manager Rob Edwards, and various other staff members responsible for coaching, scouting, sports science, and medical support.

Luton Town Football Club finishes 17th in a particular competition or league during the 2022 season.

After a slow start in the Premier League, Luton Town secured their first victory on 30 September 2023 by defeating Everton 2–1 away at Goodison Park.

Luton Town operates a Development Squad, under-18 team, and various youth programs across Bedfordshire and North Hertfordshire. The club's youth set-up includes Soccer Centres, Centres of Excellence, and an academy catering to players from under-9 to under-16 age groups.