Genomic stability relies on an effective DNA damage response (DDR), which serves as a critical barrier against tumor development. Yet, how cellular metabolism adapts to DNA damage remains largely unexplored, limiting opportunities to develop metabolism-targeted cancer therapies [Ref]. Emerging evidence suggests that DDR is closely linked to metabolic control, particularly through the restriction of glutamine (Gln) import into mitochondria, a process that supports both cell cycle arrest and DNA repair [Ref]. In this work, we identify mitochondrial Gln metabolism as a key determinant of cell fate following DNA damage. Specifically, inhibition of glutaminase (GLS)—the enzyme responsible for initiating Gln-driven anaplerosis—renders cancer cells more susceptible to DNA damage by triggering the expression of amphiregulin (AREG), which drives apoptotic cell death. Mechanistically, GLS suppression elevates reactive oxygen species (ROS), which in turn activates AREG transcription via the Max-like protein X (MLX) transcription factor. Notably, disrupting mitochondrial Gln metabolism markedly enhances chemotherapy-induced cell death in both cell culture and animal models. Together, these findings reveal a previously unrecognized role of mitochondrial Gln metabolism in DDR-induced apoptosis and point to novel metabolic strategies for improving cancer therapy.