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0 reviewsSUMMARYThe canonical model of tumor suppressor gene (TSG)-mediated oncogenesis posits that loss of both allelesis necessary for inactivation. Here, through allele-specific analysis of sequencing data from 48,179 cancerpatients, we define the prevalence, selective pressure for, and functional consequences of biallelic inactivation across TSGs. TSGs largely assort into distinct classes associated with either pan-cancer (Class 1) or lineage-specific (Class 2) patterns of selection for biallelic loss, although some TSGs are predominantly monoallelically inactivated (Class 3/4). We demonstrate that selection for biallelic inactivation can be utilized toidentify driver genes in non-canonical contexts, including among variants of unknown significance (VUSs)of several TSGs such as KEAP1. Genomic, functional, and clinical data collectively indicate that KEAP1VUSs phenocopy established KEAP1 oncogenic alleles and that zygosity, rather than variant classification,is predictive of therapeutic response. TSG zygosity is therefore a fundamental determinant of diseaseetiology and therapeutic sensitivity.