The success of cancer immunotherapy is limited to a subset of patients, highlighting the need to identify the mechanisms by which tumors evade immunity. Using a series of genome-scale CRISPR/Cas9 screens, we reveal that melanoma cells lacking HOIP, the catalytic subunit of the linear ubiquitin assembly complex, are highly susceptible to both NK and CD8+ T cell-mediated killing. This was due to increased sensitivity to the combined effect of the inflammatory cytokines, TNF and IFN-γ, released by NK and CD8+ T cells upon target recognition. Indeed, either genetic deletion or pharmacological inhibition of HOIP augmented tumor sensitivity to combined TNF and IFN-γ induced cell death. Together, we unveil a protective regulatory axis, involving tumor-expressed HOIP, which limits a transcription-dependent form of cell death that engages both intrinsic and extrinsic apoptotic machinery upon exposure to TNF and IFN-γ. Our findings highlight HOIP inhibition as a potential strategy to harness and enhance the untapped killing capacity of TNF and IFN-γ during immunotherapy.