Activated Ras requires autophagy to maintain oxidative metabolism and tumorigenesis. This study shows that oncogenes like H-rasV12 and K-rasV12 up-regulate basal autophagy, which is essential for tumor cell survival during starvation and tumorigenesis. Autophagy helps clear damaged mitochondria and maintain mitochondrial function, which is critical for Ras-driven tumor growth. Human cancer cell lines with Ras mutations commonly exhibit high basal autophagy, and reducing autophagy impairs cell growth. Autophagy is thus crucial for the survival of aggressive cancers with Ras mutations. The study also demonstrates that autophagy supports mitochondrial metabolism and energy homeostasis, and its deficiency leads to mitochondrial dysfunction, reduced TCA cycle metabolites, and increased cell death. Autophagy is required for maintaining mitochondrial function and energy levels in Ras-expressing cells. The findings suggest that targeting autophagy and mitochondrial metabolism could be a promising therapeutic strategy for cancers with Ras mutations.Activated Ras requires autophagy to maintain oxidative metabolism and tumorigenesis. This study shows that oncogenes like H-rasV12 and K-rasV12 up-regulate basal autophagy, which is essential for tumor cell survival during starvation and tumorigenesis. Autophagy helps clear damaged mitochondria and maintain mitochondrial function, which is critical for Ras-driven tumor growth. Human cancer cell lines with Ras mutations commonly exhibit high basal autophagy, and reducing autophagy impairs cell growth. Autophagy is thus crucial for the survival of aggressive cancers with Ras mutations. The study also demonstrates that autophagy supports mitochondrial metabolism and energy homeostasis, and its deficiency leads to mitochondrial dysfunction, reduced TCA cycle metabolites, and increased cell death. Autophagy is required for maintaining mitochondrial function and energy levels in Ras-expressing cells. The findings suggest that targeting autophagy and mitochondrial metabolism could be a promising therapeutic strategy for cancers with Ras mutations.