Recently, autophagy has been demonstrated to modulate tumourigenesis and the response to cancer therapy by regulating numerous cellular functions including maintenance of cell viability under metabolic stress, mitochondrial homeostasis, regulation of reactive oxygen species accumulation, maintenance of genomic integrity, protein quality control, establishment of oncogene-induced senescence and regulation of tissue inflammation and tumour immunogenicity. Autophagy determines these different phenotypes of the tumour cell via diverse effector mechanisms, either involving buffering of metabolism or sequestration of specific proteins and organelles from the cytosol. We argue that the key to understanding the net effect of autophagy in controlling tumourigenesis will be to functionally dissect these different effector mechanisms. This will be enabled by the identification of how these are regulated by intracellular signalling pathways. Further investigation of these pathways will reveal how individual autophagy outcomes might be selectively targeted for therapeutic gain.