Founded in 1957, the company's first general manager was Kirsten Flagstad, from 1958 to 1960, and placed an emphasis on presenting operas and ballets written by Norwegian composers, and Norwegian as the standard language of the opera singers. Subsequent general managers have included Bjørn Simensen. The Ballet School at the Norwegian National Opera & Ballet was founded in 1965. In January 2009, the Norwegian Opera and Ballet was reorganized, during the tenure of Tom Remlov as general managing director. The company's current general manager is Nils Are Karstad Lysø.
In the 1980s and 1990s, Den Norske Opera campaigned for a number of years for construction of a new opera house, with preference in the Bjørvika district, a harbour area of downtown Oslo. The Oslo Opera House was opened in the spring of 2008. In 2008 Radio Marconi, an Italian company, installed a seatback multimedia system, from an idea of Geir Mortil of the Norwegian National Opera & Ballet, allowing audiences to follow opera libretto in other languages in addition to the original language.
Past artistic directors of the opera company have included Paul Curran (2009-2011) and Anne Gjevang as interim director. The current artistic director of the opera is Per Boye Hansen, since August 2012. The company's current music director (opera, orchestra and concert) is the American conductor John Fiore. The company's current director of ballet is Ingrid Lorentzen, who succeeded Espen Giljane in the post. It was announced in December 2015 that Annilese Miskimmon would be taking over as opera director in August 2017.