Genetics underpins many ways in which individuals differ. The purpose of this paper is to advance a model with testable hypotheses regarding the cause of the genetic basis of personality. We proceed by developing the suggestion that diversity in personality genes evolved to constrain parasitic elements of culture and discuss its implications. In particular, a critical test of this hypothesis is whether personality genes show fluctuating linkage disequilibrium and a dispersed distribution throughout the genome. It is further suggested that this Red Queen process has facilitated the evolution of intelligence and allowed a higher mutation rate in relevant genes. The model’s empirical predictions are discussed in the context of alternative explanations, including those regarding intragenomic conflict, economics, and heterozygote advantage.