The club originates from Aghdam in the Karabakh (Azerbaijani: Qarabağ) region, but has not played in its hometown since 1993 due to the First Nagorno-Karabakh War.

Qarabağ is the first Azerbaijani team to advance to the group stage of the higher UEFA Champions League, competing in the 2017–18 season.

The club was founded in 1951 as Mehsul after the Aghdam city stadium was built;[8][9][10] there then began a serious effort towards the creation of a professional football team.

[19] In 2008, former Azerbaijani football star Gurban Gurbanov was appointed as head coach after the unexpected departure of Rasim Kara to Khazar Lankaran one week before the start of the 2008–09 season.

Led by Gurban Gurbanov, Qarabağ have ignored a common strategy in Azerbaijani football: eschewing foreign signings in favour of nurturing local talent.

[3] Gurbanov brought with him a tiki-taka style of play, characterised by short passes, long periods of build-up and players interchanging positions.

[23] In 2010, the club set an Azerbaijani record for the most significant win in a European competition by beating Metalurg Skopje 4–1 in Baku and eliminating Wisła Kraków to reach the play-offs for the second year in succession.

[27] The 2011–12 season ended in disappointing style for Qarabağ, however, as they finished in fourth place, leaving the club without European competition.

[31] A month later, by beating Red Bull Salzburg, the club became first Azerbaijani side to win in the third round of UEFA Champions League.

[39] Despite losing 2–1 in the second leg, Qarabağ won on away goals and became the first Azerbaijani team to reach the group stages of the UEFA Champions League.

[40] They were drawn in Group C alongside Chelsea, Atlético Madrid and Roma, where they managed to obtain two points in six games after two draws and four losses.

[41] In July and August 2021, Qarabağ secured their first participation in the group stage of UEFA Europa Conference League.

On 27 August, Qarabağ was drawn on Group H of the 2021–22 UEFA Europa Conference League alongside Basel, Kairat and Omonia.

[47] The club have previously used Guzanli Olympic Stadium, which is situated in Quzanlı, the most populous municipality in the Agdam Rayon of Nagorno-Karabakh, Azerbaijan.

[55] The club is a sole remnant of the past and a living symbol of hope and pride for over half a million Azerbaijani internally displaced people.

In recent years, thanks to achievements on the pitch, the club has been able to inspire and initiate special youth projects enforcing stability and development in the IDP-settlements near the border of Nagorno-Karabakh.

[20][63][64] Qarabağ's traditional kit alludes to the club's location in Nagorno-Karabakh with the black and white representing light and darkness respectively.

The top transfer was agreed in January 2025 when 28 years old Brazilian forward Juninho moved to Flamengo for a fee €5.00 million.

[83] In October 2020, amid the Nagorno-Karabakh war, the Armenian Football Federation called for sanctions against Qarabağ after the club's PR and media manager Nurlan Ibrahimov posted a hate message on a social media network calling to "kill all the Armenians, old and young, without distinction".

[84] UEFA announced a temporary suspension of the club's official from any football-related activity for "racist and other discriminatory conduct” targeting Armenians.

[85] Qarabag issued a statement saying Ibrahimov had been traumatised by watching the news of the Ganja and Barda missile attacks, while also urging its employees to "refrain from such sharing in this sensitive period, adhere to the principles of humanism and fully comply with the laws of our state".