Natural selection should favour litter sizes that optimise trade-offs between brood-size and offspring viability. Across the primate order, the modal litter size is one, suggesting a deep history of selection favouring minimal litters in primates. Humans, however – despite having the longest juvenile period and slowest life-history of all primates – still produce twin births at appreciable rates, even though such births are costly. This presents an evolutionary puzzle. Why is twinning still expressed in humans despite its cost? More puzzling still is the discordance between the principal explanations for human twinning and extant empirical data. Such explanations propose that twinning is regulated by phenotypic plasticity in polyovulation, permitting the production of larger sib sets if and when resources are abundant. However, comparative data suggest that twinning rates are actually highest in poorer economies and lowest in richer, more developed economies. We propose that a historical dynamic of gene–culture co-evolution might better explain this geographic patterning. Our explanation distinguishes geminophilous and geminophobic cultural contexts, as those celebrating twins (e.g. through material support) and those hostile to twins (e.g. through sanction of twin-infanticide). Geminophilous institutions, in particular, may buffer the fitness cost associated with twinning, potentially reducing selection pressures against polyovulation. We conclude by synthesising a mathematical and empirical research programme that might test our ideas.