Autophagy, a catabolic process that involves the self-digestion of cellular organelles, plays a dual role in mammary tumorigenesis. On one hand, it acts as a haploinsufficient tumor suppressor mechanism by regulating the essential autophagy regulator *beclin1*. On the other hand, defective autophagy can sensitize mammary epithelial cells to metabolic stress and accelerate lumen formation in mammary acini. This study demonstrates that allelic loss of *beclin1* and defective autophagy activate the DNA damage response, promote gene amplification, and synergize with defective apoptosis to enhance mammary tumorigenesis. The findings suggest that autophagy limits metabolic stress to protect the genome, while defective autophagy increases DNA damage and genomic instability, ultimately facilitating breast cancer progression. These results provide insights into the therapeutic implications of targeting autophagy in breast cancer, highlighting the potential benefits of combining autophagy promotion with metabolic stress-inducing agents.Autophagy, a catabolic process that involves the self-digestion of cellular organelles, plays a dual role in mammary tumorigenesis. On one hand, it acts as a haploinsufficient tumor suppressor mechanism by regulating the essential autophagy regulator *beclin1*. On the other hand, defective autophagy can sensitize mammary epithelial cells to metabolic stress and accelerate lumen formation in mammary acini. This study demonstrates that allelic loss of *beclin1* and defective autophagy activate the DNA damage response, promote gene amplification, and synergize with defective apoptosis to enhance mammary tumorigenesis. The findings suggest that autophagy limits metabolic stress to protect the genome, while defective autophagy increases DNA damage and genomic instability, ultimately facilitating breast cancer progression. These results provide insights into the therapeutic implications of targeting autophagy in breast cancer, highlighting the potential benefits of combining autophagy promotion with metabolic stress-inducing agents.