The theoretical heuristic of assuming distinct alleles (or genotypes) for alternative phenotypes is the foundation of the paradigm of evolutionary explanation we call the Modern Synthesis. In modeling the evolution of sociality, the heuristic has been to set altruism and selfishness as alternative phenotypes under distinct genotypes, which has been dubbed the “phenotypic gambit.” The prevalence of the altruistic genotype that is of lower evolutionary fitness relative to the alternative genotype for non-altruistic behavior in populations is the basis of the (...) “paradox of altruism.” I show in this article that the assumption of contrasting genotypes for altruism and selfishness in our “phenotypic gambit” is inconsistent with the empirical data when viewed in the light of today’s post-Mendelian understanding of gene expression. I demonstrate that however nuanced and sophisticated the models may have become today, they are still rooted in that fundamentally problematic assumption. I then offer a genetic conception of altruism that best fits the field data. (shrink)