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Macroautophagy is the process by which cells package and degrade cytosolic components, and recycle the breakdown products for future use. Since its initial description by Christian de Duve in the 1960s, significant progress has been made in understanding the mechanisms that underlie this vital cellular process and its specificity. Furthermore, macroautophagy is linked to pathologic conditions such as cancer and is being studied as a therapeutic target. In this review, we will explore the connections between autophagy and cancer, which are tumor- and context-dependent and include the tumor microenvironment. We will highlight the importance of tumor compartment-specific autophagy in both cancer aggressiveness and treatment.