The success of cancer immunotherapy is limited to a subset of patients, highlighting the need to identify the processes by which tumors evade immunity. Using whole-genome CRISPR/Cas9 screening, we reveal that melanoma cells lacking HOIP, the catalytic subunit of the linear ubiquitin chain assembly complex (LUBAC), are highly susceptible to both natural killer (NK) and CD8+ T cell-mediated killing. We demonstrate that HOIP-deficient tumor cells exhibit increased sensitivity to the combined effect of the inflammatory cytokines, tumor necrosis factor (TNF) and interferon-gamma (IFN-γ), secreted by NK and CD8+ T cells upon target recognition. Both genetic deletion and pharmacological inhibition of HOIP augments tumor cell sensitivity to combined TNF and IFN-γ. Together, we unveil a protective regulatory HOIP-cytokine axis, 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/LUBAC inhibition as a potential strategy to harness and enhance the killing capacity of TNF and IFN-γ during immunotherapy, where amounts of these cytokines are elevated.