T cells of the adaptive immune system monitor protein degradation products via their presentation on major histocompatibility complex (MHC) molecules to recognize infected cells. Both macroautophagy and endocytosis target intra- and extracellular constituents, respectively, for lysosomal degradation. This results in antigen processing for MHC presentation and influences the trafficking of MHC molecules. This review will discuss recent evidence that the molecular machinery of macroautophagy regulates also endocytosis at the level of phagosome maturation and cell membrane internalization. These non-canonical functions of this machinery affect both MHC class I and II restricted antigen presentation to CD8+ and CD4+ T cells, respectively, and should be harnessed to improve immune responses against infectious diseases and cancer.