Oncogenic RAS is present in 30% of human cancers; however, cancer is a cooperative process and RAS-activating mutations alone are insufficient to promote tumourigenesis. In a loss-of-function screen, several genes involved in the autophagy pathway were revealed to cooperate with RAS when knocked down, implicating autophagy as a novel suppressor of RAS-driven tumourigenesis. Furthermore, loss of autophagy has been shown to increase oxidative stress and activate cellular stress response pathways, suggesting autophagy limits these processes as a potential RAS tumour-suppressing mechanism. To investigate the interplay between autophagy and oxidative stress in RAS-driven cancers, a screen using Drosophila RNAi lines of novel RAS tumour-suppressing genes was performed in tissues with constitutively active RAS. This reverse genetics approach to assess gene function revealed several genes that putatively act as regulators of autophagy. Similarly, RAS-activated autophagy-deficient tissues were shown to accumulate oxidative stress both cell and non-cell autonomously, and the Wingless intracellular signalling pathway was dysregulated through this loss in autophagy. These findings further characterise a complex interplay between oncogenic RAS, autophagy, and oxidative stress that has previously been implicated in tumourigenesis. Importantly, understanding this interplay and identifying genes that have a regulatory function impacting autophagy is crucial for the development of therapeutics targeting this pathway in RAS-driven epithelial tumourigenesis.