The club has been functioning since 1997, but initially it had a different name. The club originally shared named with “Khazar University”, the first private university in Azerbaijan which founded the club. The club debuted in the amateur league in 1997. In 1999, “Khazar University” began to play in the Azerbaijan Premier League and club ended its debut in 11th place. In subsequent years, “Inter Baku” finished in 7th place (2000/01 season) and 3rd place (2003–04 season).

In 2003–04 season the team performed well and ended the season in fourth place. This result earned the club the right to play in the UEFA Intertoto Cup for the first time. In the first round of the 2004 Intertoto Cup, “Khazar University” defeated “Bregenz” of Austria 3:0 in the first leg on a forfeit and 2:1 in the second leg. In the second round of the tournament, “Khazar University” played “Tampere United” from Finland. The club lost the first game 0:3, but won the return leg held in Baku, 1:0. “Khazar University” lost the tie on aggregate and was out of its first Intertoto cup.

In summer of 2004, all rights of the “Khazar University” club were transferred to newly created “Inter” Baku Professional Football Club, and the team participated in the 13th championship of the Azerbaijani Premier League under the name of “Inter Baku”. Later in 2004, certain structural changes were made in the club's management, and Inter Baku was renamed the “Inter” Professional Sport Club, finishing the 2004–2005 season in seventh place. Inter's progression up the standings continued in the 14th iteration of the Azerbaijan Premier League when Inter finished in fourth place.

The club repeated its performance with fourth again in 2006–07 before winning the league championship in 2007–08. Following its victory in the domestic league, Inter qualified for its first-ever appearance in the UEFA Champions League in 2008 and advanced to the second qualifying round by defeating “Rabotnički” of the Republic of Macedonia on away goals.

2009 saw “Inter Baku” retain the Azerbaijan Premier League title, securing it second time in club's history. The club's Champions League campaign was less successful – barely losing to “Lech” Poznań away in penalties. In 2011, “Inter Baku” also managed to win the CIS Cup after defeating “Shakhtsyor” Salihorsk in the final.

In 2012, the club recorded Azerbaijani record for the biggest win in a European competition by beating “Narva Trans” 5–0 in Estonia.The club had started the 2013–14 seasonwith a three-game losing streak, setting a record for worst start to a season in its history. However, the team managed to clinch second spot in the league.

İn 2013-14 UEFA Europa League “Inter Baku” won Moldovian team “Tiraspol” on away goals in the first qualifying round. But in next round “Inter” could not beat “Elfsborg” акщь Swees.

In 2015-16 Europa League “Inter Baku” beat Albanian side Laci on away goals in the first qualifying round, before overcoming Icelandic outfit FH 4-3 on aggregate in the next round. In next round “Inter Baku” met Athletic Bilbao. First match ended with score 2:0 in favor Spain club. In second leg the match was ended with score 0-0. 

Successes

CIS Cup

  • Winner-2011
  • ½ final-2009

Azerbaijan Championship

  • Gold medal(2)- 2007/2008, 2009/2010
  • Silver medal(3)- 2008/2009, 2013/2014, 2014/2015
  • Bronze medal (2)- 2011/2012, 2012/2013

Azerbaijan Cup

  • Fınal(4)- 2004/2005, 2007/2008, 2008/2009, 2010/2011
  • Winner-2017-2018