The E6-Associated Protein (E6AP) is an E3 ubiquitin ligase, initially characterized for its role in p53 degradation in HPV-infected cells. We recently demonstrated that E6AP-deficient cells evade oncogene and stress-induced senescence. We now report that E6AP knockout MEFs show reduced levels of the genes encoded by the INK4/ARF locus, providing a molecular mechanism by which E6AP controls cellular senescence. The INK4/ARF locus is the most frequently inactivated locus in human cancer and it encodes for the key tumor suppressors p15INK4b, p16INK4a and p19ARF. Specifically, p16INK4a is lost at high frequency in several cancers, including non-small cell lung cancer (NSCLC), and while hypermethylation is responsible for its loss in nearly half the cases, the mechanism for the remaining cases is unknown. Our results demonstrate that E6AP regulates the INK4/ARF locus by inhibition of Cdc6, a key repressor of this locus. These findings are further supported by the use of a genetically engineered mouse model of NSCLC driven by mutant KRas, where we demonstrate that gene targeting of E6AP increases growth and progression of NSCLC. Importantly, we defined a subset of NSCLC patients with E6AP low/Cdc6 high/p16 low expression profile signature, which is associated with poor prognosis and a low frequency of p16INK4a hypermethylation. Overall, our study demonstrates a role for E6AP in the maintenance and progression of NSCLC and provides a novel alternative molecular explanation for the silencing of the INK4/ARF locus in cancer.