Zvyagintsev was born in Novosibirsk, Siberia. At the age of 20 in 1984 he graduated from the drama school in Novosibirsk as an actor. Since 1986 he has lived in Moscow where he continued his studies at the Russian Academy of Theatre Arts until 1990. From 1992 to 2000 he worked as an actor for film and theater. In 2000 he began to work for the TV station REN TV and directed three episodes of the television series The Black Room.

In 2003, he directed his first feature film The Return, which received several awards, including a Golden Lion at the Venice Film Festival. His second feature film The Banishment premiered at the 2007 Cannes Film Festival and was nominated for a Palme d’Or. In 2008, he directed “Apocrypha”, a short segment for the film New York, I Love You. The segment was eventually cut from the film’s theatrical release but is included on the DVD.

His 2011 film, Elena, premiered at the 2011 Cannes Film Festival, in the Un Certain Regard section, where it won the Jury Prize.

His 2014 film Leviathan was selected to compete for the Palme d’Or in the main competition section at the 2014 Cannes Film Festival, where Zvyagintsev and Oleg Negin won the award for Best Screenplay for the film. Leviathan won the Golden Globe Award for Best Foreign Language Film and was nominated for the Academy Awards for Best Foreign Language Film. In 2015, Zvyagintsev was a jury president of the 18th Shanghai International Film Festival.

His most recent film Loveless won the Jury Prize at the 2017 Cannes Film Festival. It went on to win the Best Film at the 2017 London Film Festival, making him the second director to have won the award twice, having previously been honoured for Leviathan. In November 2017, the film won three awards at the Golden Unicorn Awards in London: Best Film, Best Screenplay, Best Actress.