After graduating from Russian Theatre Academy in 1993, he started staging opera productions and theatre productions in Russia and abroad. Usually, he creates the scenic design and costumes for his productions.

He is laureate of numerous prizes of Russian theatre, among them the national prize Golden Mask, which he received several times. As well, he was nominated in Russia for The Best Stage Director of the Year for several operatic productions. In 2009 he received the Franco Abbiati Italian music critic prize.

Among his most important productions are: The Rake’s Progress by Stravinsky, Eugene Onegin by Tchaikovsky (Bolshoi Theatre, Moscow), The Legend of the Invisible City of Kitezh and Maid Fevronia by Rimsky-Korsakov, A life for the Tsar  by Glinka, Tristan and Isolde by Wagner (Mariinsky Theatre, Sankt Petersburg),  Aida by Verdi (Novosibirsk State Opera), Boris Godunov by Moussorgsky (Staatsoper Unter den Linden, Berlin), Khovanshchina by Moussorgsky (Bavarian State Opera, Munich), The Gambler by Prokofiev (Staatsoper Unter den Linden in Berlin and Teatro alla Scala in Milan), Macbeth by Verdi at the Paris National Opera and Wozzeck by Berg at Bolshoi Theatre Moscow, Dialogs of Carmelites by Poulenc at the Bavarian State opera, Don Giovanni by Mozart at Aix-en-Provence Festival.

In 2011 Dmitri Tcherniakov made his London debut with Simone Boccanegra by Verdi at the English National Opera. He opened the old/new Bolshoi Theater with Ruslan and Ludmila by Glinka in November 2011.

He staged The Legend of the Invisible City of Kitezh and the Maiden Fevroniya by Nikolai Rimsky-Korsakov at the De Nederlandse Opera Amsterdam in 2012 and was named “stage designer of the year” by the famous magazine “Opernwelt”. He created Il trouvatore at Théâtre Royal de la Monnaie Belgique and Jenufa at the opera house Zürich.

In 2013 he opened the new season at the Staatsoper Berlin with Tzar’s bride and then the Verdi-Year with a new production of La Traviata at La Scala in Milano. Dmitri Tcherniakov made his debut at the Metropolitan Opera with Prince Igor in 2014. In the same year, he showed his interpretation of Tzar’s bride at the Staatsoper Berlin. In the theatre season 2014/15 Dmitri Tcherniakov staged Don Giovanni at the opera in Toronto, Parsifal at the Staatsoper Berlin, Lulu at the Bayrischen Staatsoper Munich. In 2015/16 he staged Lady Macbeth von Mzensk at ENO London (co-production with Lyon Opera), Iolanta/Nußknacker in Paris and Pelléas et Mélisande in Zurich. The season 2016/2017 started with Bluebeard’s Castle / Senza Sangue at the Staatsoper Hamburg. He also staged Prince Igor at the Dutch National Opera Amsterdam, Snegourochka at the Opéra national de Paris and Carmen in Aix en Provence. In 2017/2018 he directed the very successful production of Tristan and Isolde at the Staatsoper Berlin.

The season 2018/2019 started with Les Troyens at the Opera National de Paris, Opera Bastille, and continued with Prokofiew’s Betrothal in a Monastery at the Staatsoper Berlin and Rimski-Korsakow’s Le conte du Zar Saltan at La Monnaie in Brussel.  In 2019 he directed The Makropulos Case at the Zurich Opernhaus, and in 2021 he directed Der Fliegender Holländer at the Bayreuther Fetspiele and Elektra at the Staatsoper Hamburg.