Bekmambetov was born on 25 June 1961, in the city of Guryev (now Atyrau). His father, Nuruakhit Bekmambetov, worked in the energy management of Guryevenergo in leading positions. According to Timur, he was the chief power engineer of Western Kazakhstan. His mother, Mira Bogoslovskaya, was the deputy editor of the regional newspaper Prikaspiyskaya Kommuna, where she was in charge of the party building department. He has Kazakh ancestry on his father’s side, and Russian-Jewish ancestry on his mother’s side.

After graduation from school, Bekmambetov entered the Moscow Power Engineering Institute in 1979. In 1980, he left the institute on the eve of the 1980 Summer Olympics. 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, where he graduated in 1987 with a degree in theater and cinema set design. It was during this period that Bekmambetov served in the Soviet Army, which inspired him to write Peshavar Waltz.

Between 1992 and 1997, Bekmambetov was directing commercials and was one of the directors for Bank Imperial’s award-winning popular World History ads. In 1994, he founded Bazelevs Group, an advertising and films production, distribution and marketing company.

Bekmambetov’s first feature, Peshavar Waltz, (1994) was a violent and realistic look at the war between the USSR and Afghanistan. The film was dubbed in English as Escape from Afghanistan and released direct-to-video by Roger Corman in 2002. Bekmambetov next produced and directed an eight-parts miniseries for television entitled Our ’90s. Bekmambetov then returned to directing features, with Roger Corman produced The Arena, which starred Karen McDougal and Lisa Dergan. The film was a remake of The Arena of the same name. In 2001, Bekmambetov directed and co-produced (with Bahyt Kilibayev) the film GAZ-Russian Cars.

In 2004, Bekmambetov wrote and directed Night Watch (2004), a popular Russian fantasy film based on the book by Sergey Lukyanenko. The film was extremely successful in Russia, and at the time became its highest-grossing released ever, making US$16.7 million in Russia alone, more than The Lord of the Rings: The Fellowship of the Ring. Night Watch is also notable for establishing Konstantin Khabensky as a star. The sequel to Night Watch, Day Watch (2006), was likewise written and directed by Bekmambetov. The two films attracted the attention of Fox Searchlight Pictures, which paid $4 million to acquired worldwide distribution rights (excluding Russia and the Baltic states).

In 2010, Bekmambetov produced and was one of the directors of Yolki a.k.a. “The Six Degrees to Celebration” (English title) which became the second highest-grossing Russian movie in Russian box office history. The film later spawned five sequels and one spin-off. In February 2011 Bazelevs released the Bekmambetov-produced Lucky Trouble starring Milla Jovovich and Konstantin Khabensky) – the film was Jovovich’s film debut in Russian.

Bekmambetov produced Apollo 18 in 2011, along with The Weinstein Company, a found footage science fiction thriller, and The Darkest Hour, a science fiction film set in Moscow and produced by New Regency.

In 2012, Bekmambetov directed and produced the live-action adaptation of the Seth Grahame-Smith novel Abraham Lincoln, Vampire Hunter, also produced by Tim Burton and Jim Lemley. He was awarded the International Filmmaker of the Year award in 2012 by the National Association of Theatre Owners.

Variety (Russian Edition) named Bekmambetov one of the most commercially successful Russian directors of the decade in 2013. He was placed on top of the list ($137.1M Gross) with Fyodor Bondarchuk ($53.47M Gross), Sarik Andreasyan ($42.92M Gross), Pyotr Buslov ($42.21M Gross) and Marius Weisberg ($36.85M Gross).

From 2015, Bekmambetov has produced a number of computer screen films. He has referred to the genre as Screen Life and Screen Movies.

In 2015 Bekmambetov produced the horror film Unfriended which was directed by Levan Gabriadze. He produced the 2016 comedy Hack the Bloggers by Maksim Sveshnikov.

Bekmambetov directed Ben-Hur in 2016, which was the fifth film adaptation of the novel Ben-Hur: A Tale of the Christ by Lew Wallace. The picture fell below box-office expectations.

In 2017 Bekmambetov served as producer on the biographical picture The Age of Pioneers telling the story of cosmonaut Alexei Leonov who performed the first spacewalk in history. The film received positive reviews. He also produced another biopic in the same year – The Current War which is about the war of currents between Thomas Edison and George Westinghouse.

In 2018, Bekmambetov produced three thriller films, Searching, directed by Aneesh Chaganty, Profile, directed by himself, and the Unfriended sequel, Unfriended: Dark Web.