He was deported from Moscow on the grounds of being "unreliable" and moved to Tashkent, Uzbek SSR, to study at the Alexander Ostrovsky Theatrical and Artistic Institute, from which he graduated in 1987 with a degree in theater and cinema set design.

Bekmambetov started his career in the late 1980s as a production designer at the Ilkhom Theatre in Tashkent, Uzbekistan, and at Uzbek national film studio Uzbekfilm.

[8] The Russian blockbuster epic attracted the attention of Fox Searchlight Pictures, which paid US$4 million to acquire the worldwide distribution rights (excluding Russia and the Baltic states).

[12] Bekmambetov's Hollywood directorial debut was Universal's action thriller Wanted (2008), an adaptation of the graphic novel series created by Mark Millar and J. G.

[14] In 2009, alongside Tim Burton and Jim Lemley, Bekmambetov produced an animated film titled 9 (2009), the story of a rag doll in a post-apocalyptic world, directed by Shane Acker.

In 2012, Bekmambetov directed and produced the live-action adaptation of Seth Grahame-Smith's novel – Abraham Lincoln, Vampire Hunter,[17] together with Tim Burton and Jim Lemley.

In 2017, Bekmambetov produced the historical drama The Current War starring Benedict Cumberbatch, Tom Holland, Nicholas Hoult and Michael Shannon.

In 2021, Deadline announced that Bekmambetov would be bringing to the screen a new universe based on the unexploited works in the horror genre by the Marvel Сomics creator Stan Lee.

In December 2022, Bekmambetov sold the Bazelevs film studio in Russia to its general producer, Lala Rustamova, and commercial director, Timur Asadov.

Inspired by the 2015 nonfiction bestseller In the Skin of a Jihadist by a French journalist Anna Erelle, Profile won the 2018 Audience Award by Berlin Film Festival.

[25] Bekmambetov's recent screenlife production, R#J, a Gen Z adaptation of Shakespeare's Romeo and Juliet, premiered at Sundance 2021 and won a special prize at SXSW.

[27][28] Bekmambetov is married to the Russian urbanist Natalia Fishman-Bekmambetova, who worked on the restoration of Gorky Park in Moscow and the renovation of the city of Kazan.