Jonathan Glazer was born into a Jewish family in London, and studied in a Jewish school. After studying theatre design at Nottingham Trent University, Glazer started out directing theatre and making film and television trailers, including award-winning work for the BBC. In 1993 he wrote and directed three short films of his own ("Mad", "Pool" and "Commission"), and joined Academy Commercials, a production company based in London. He has directed popular campaigns for Guinness (Swimblack and Surfer) and Stella Artois (Devil's Island). Since the mid-1990s he has directed a number of music videos, and was named MTV Director of the Year 1997. His work in these areas is often noted for its originality.

In 2000, he directed his first feature, the British gangster film Sexy Beast, starring Ray Winstone and Ben Kingsley. In 2004 he directed his second feature film Birth, starring Nicole Kidman, in the United States.

In 2001, Glazer directed the "Odyssey" spot for Levi Strauss Jeans. In 2006, he directed the second Sony BRAVIA TV advertisement, which took 10 days and 250 people to film. It was filmed at an estate in Glasgow, and featured paint exploding all over the tower blocks. Later the same year he was commissioned to make a television advert for the new Motorola Red phone. The advertisement, showing two naked black bodies emerging from a lump of flesh rotating on a potter's wheel, was due to air in September 2006 but was shelved by Motorola. The advertisement was to benefit several charities in Africa.

In 2013 he directed Under the Skin, a loose adaptation of Michel Faber's science fiction novel of the same name starring Scarlett Johansson. The film premiered at the 2013 Telluride Film Festival and received a theatrical release in 2014, garnering positive, sometimes ecstatic reviews.