Oliver von Dohnányi studied in the faculty of music at the Academy of Performing Arts Prague with Václav Neumann and later at Vienna's University of Music and Performing Arts with Otmar Suitner. Directly after his studies, he was appointed to a conducting position with the Czechoslovak Radio Symphony Orchestra (since renamed the Slovak Radio Symphony Orchestra). Seven years later, in 1986, he became the music director of the Slovak National Theatre in Bratislava, the youngest in the institution's history. There he conducted Madama Butterfly, Aida, La bohème, Rusalka, Macbeth, Tosca, Il barbiere di Siviglia, Bellini's La sonnambula, Gounod's Faust, Slovak composer Eugen Suchoň's The Whirlpool, along with many other works. In addition, he toured regularly, visiting Spain, Bulgaria, China, Hungary, Germany and the Netherlands. Starting in 1993, he also took up conducting the Slovak Philharmonic alongside his duties with the opera orchestra.

He later switched his principal base of operations from Bratislava to Prague, where he joined the Czech National Theatre as a guest conductor before eventually being appointed music director. There his repertoire included La bohème, Il barbiere di Siviglia, Il turco in Italia, The Bartered Bride, Rigoletto, La traviata, Rusalka, Samson et Dalila, Macbeth, Smetena's Libuše, Don Giovanni, Le nozze di Figaro, Die Zauberflöte, Don Pasquale, Tosca, Norma, The Whirlpool, Aida, along with ballet pieces like Prokofiev's Romeo and Juliet and Cinderella. During this same period, he also had many foreign engagements as a guest conductor, including Christopher Alden's 2012 production of Norma, which won the British Opera Award for “best opera of 2012”.

In 2015, he also conducted Thaddeus Strassberger's new version of the Philip Glass opera Satyagraha at Moscow's Bolshoi Theatre. The production won two Golden Mask awards.
He has also worked with various record companies, having recorded on the Naxos, Lyra, Opus, Audiophon, Panton, Supraphon, Marco Polo and Novalis labels.
In the 2015/16 season, von Dohnányi joined Yekaterinburg's Ural Opera and Ballet Theatre as first conductor.

In the 2017/18 season, he conducted the following new productions: Leoš Janáček's opera Kát'a Kabanová at the Seattle Opera, Das Liebesverbot at the Teatro Colón in Buenos Aires, Les Huguenots at the Hungarian State Opera, Carmen at the New Zealand Opera and Die Zauberflöte, Rusalka and Bohuslav Martinů's The Greek Passion in Yekaterinburg.

In 2018, he was presented the highest award of Russia's national theatres: the Golden Mask in the category of “best opera conductor“.