Social interaction is a sophisticated behavior that is impaired in individuals with autism spectrum disorders (ASD). Because of its complexity, the mechanisms underlying typical social interactions, as well as the development of ASD pathology, remain poorly understood, and effective treatments are still lacking. Autophagy is a lysosomal degradation pathway important for intracellular protein homeostasis and is controlled by ~40 autophagy-related proteins, including the Beclin family member BECN1. Biallelic variants or reduced expression of autophagy genes, including Becn1, Atg7 and Atg8, are recently discovered in complex neurodevelopmental syndromes in humans; however, the underlying pathogenic mechanism is mysterious. While autophagy proteins are generally thought to participate in lysosome-mediated degradation, emerging evidence indicates that they may have more diverse non-canonical roles beyond this function. Here we discover that the autophagy protein BECN1 is a regulator of social behavior by stabilizing excitatory receptor neurotransmission, via a crosstalk with the ubiquitin-proteasomal machinery. Proteomic and biochemical studies identify BECN1 as a binding partner of both an E3 ubiquitin ligase UBE3A and its substrate Arc. Accumulation of Arc is associated with excessive endocytosis and reduced levels of excitatory receptors in ASD. We reveal that BECN1 serves as an adaptor for UBE3A-mediated Arc polyubiquitination and proteasomal degradation, thereby maintaining postsynaptic receptor levels. Using electrophysiology and behavioral approaches, we found that loss of BECN1 in hippocampal neurons decreases excitatory neurotransmission and impairs social interaction, resembling ASD-associated phenotypes. Thus, our study demonstrates that BECN1 is a novel regulator of social behavior by promoting UBE3A-mediated Arc degradation and ensuring cell-surface excitatory receptor stability and neurotransmission in the hippocampus.