Pyunik was founded in 1992 by Armenian football legend Khoren Oganesian and originally named Homenetmen Yerevan.

[8] The club won the first Armenian Premier League competition held in 1992 which it shared with Shirak since both teams were tied on points.

Following the change of name, Pyunik went on to win the 1995–96 Armenian Premier League and end the season with a 59-match unbeaten streak.

[10] Pyunik also won the 1996-97 Armenian Premier League securing itself another chance at qualifying for an international cup playoffs the following year.

Pyunik secured a comeback to professional football following its absorption of FC Armenicum, a newly promoted team to the Armenian Premier League.

[17] On 20 July 2020, Artak Oseyan was announced as Pyunik's new manager,[18] but left his role as head coach on 13 December 2020.

Subsequently, Pyunik dropped into the play-off round of the Europa League, where they played against the Moldovan side Sheriff Tiraspol.

After a defeat away against Basel on the first matchday, Pyunik faced Slovan Bratislava in their first home match in Yerevan, which they won thanks to goals from Artak Dashyan and Yusuf Otubanjo.

On 31 December 2024, Pyunik released a statement stating that ownership of the club had passed from Artur Soghomonyan to Anton Farber.

Following the club's reappearance in 2001, Pyunik introduced its iconic logo design which included a bold letter P placed on top of a football.

This change resulted unpopular among the fans and Pyunik introduced a new badge in 2019, this time returning to its original round shape with a predominantly blue logo and a red phoenix in the center.

Between 2013 and 2017, the Yerevan Football Academy served as a home venue for all domestic competitions, while still using the Republican Stadium for international fixtures.

[28] Notable players from the youth academy include Henrikh Mkhitaryan, Robert Arzumanyan, Karlen Mkrtchyan, Edgar Manucharyan, Varazdat Haroyan and Gevorg Ghazaryan.