It is headquartered in the Opera House on the coast of the Töölönlahti bay in Töölö, which opened in 1993, and is state-owned through Senate Properties.

Prior to that, opera had been performed in Finland sporadically by touring companies, and on occasion by Finnish amateurs, the first such production being The Barber of Seville in 1849.

A group of notable social and cultural figures, led by the international star soprano Aino Ackté, founded the Domestic Opera in 1911.

In 2020, in response to the COVID-19 pandemic and the cancellation of many of its planned productions, Finnish National Opera commissioned, created, and produced Covid fan tutte, a comic opera using music from Mozart's Cosi fan tutte, starring a Finnish cast and premiering in late August 2020 with social distancing restrictions.

Past music directors and chief conductors have included Armas Järnefelt (1932–36), Tauno Pylkkänen (1960–1967), Okko Kamu (1996–2000), Muhai Tang (2003–2006),[4] and Mikko Franck (2006–2013).

[9] In December 2017, the company announced the appointment of Madeleine Onne as the next artistic director of Finnish National Ballet, effective August 2018.