The greatest club success was in the 2002–03 season when they finished runners-up in the Croatian Cup, losing to Hajduk Split 5–0 on aggregate.

The group of die hard fans are referred to as the Demoni, and are known for their explosive chants and celebrations as well as their extreme pride for the club.

In summer 2018, club's ownership changed once again, this time to Basque consortium Baskonia - Alavés Group which acquired the majority share package and became sole owner of NK Istra 1961.

Istra 1961 play their home matches at the recently renovated Stadion Aldo Drosina, which has a capacity of approximately 10,000 spectators.

The club stopped functioning shortly thereafter, but was restarted by Silvan Farangua and Ivan Čehić in 1964, when they played in the Pula county league.

[5] Two years later in the 2002–03 season, under the leadership of manager Elvis Scoria, Istra played in the final of the Croatian Cup, losing to Hajduk Split.

It is the only time, in the history of Croatian football, that a Druga HNL league club played in the cup final.

The club played first league football for the first time in their history in the 2004–05 season, and managed their first Prva HNL win against Osijek in the fourth gameweek.

[9] The intervention of the Istria govurner and arrival of new sponsors managed to save the club, while the new president became Darko Jergović.

[14] In June 2018, NK Istra was bought by the Baskonia-Alaves Group, who acquired the majority stake in the club, buying a total of 85% of the shares.

[15][16] On 14 April 2021, Istra 1961 repeated the success of the 2013–14 season, qualifying for the final of the Croatian Cup, with a 3–2 home victory over Rijeka in the semifinal.

On 26 November 2023, Istra 1961 broke record for number of people attending their home game at Stadion Aldo Drosina.

The following are lists of top players in terms of number of appearances and goals for Istra 1961 in the Croatian First Football League, as of 3 June 2023.