Aster was born into a Jewish family in New York City on July 15, 1986, the son of a musician father and a poet mother. He has a younger brother. He recalled going to see his first movie, Dick Tracy, when he was four years old. The film featured a scene where a character fired a tommy gun in front of a wall of fire. Aster reportedly jumped from his seat and "ran six New York City blocks" while his mother tried to catch him. In his early childhood, Aster's family briefly lived in England, where his father opened a jazz nightclub in Chester. Aster enjoyed living there, but the family returned to the U.S. and settled in New Mexico when he was 10 years old.
As a child, Aster became obsessed with horror films, frequently renting them from local video stores: "I just exhausted the horror section of every video store I could find. I didn't know how to assemble people who would cooperate on something like that. I found myself just writing screenplays." In 2004, he enrolled at the College of Santa Fe, where he studied film. After graduating in 2008, he was accepted into the 2010 class of fellows at the AFI Conservatory graduate program, where he earned an MFA with a focus in directing.
Aster's debut film was the short film Tale of Two Tims, which he wrote at College of Santa Fe and submitted to American Film Institute. This garnered him a fellowship into the graduate directing program at the AFI Conservatory. Aster followed up with several AFI cycle films, along with comedic shorts made with industry friends like TDF Really Works in 2011. Aster then followed up with a breakout short film The Strange Thing About the Johnsons, which stars Billy Mayo, Brandon Greenhouse, and Angela Bullock as members of a suburban family in which the son is involved in an abusive incestuous relationship with his father.

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