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A central challenge for biology is to reveal how different levels of biological variation interact and shape diversity. However, recent experimental studies have indicated that prevailing models of evolution cannot readily explain the link between micro- and macroevolution at deep timescales. Here, we suggest that this paradox could be the result of a common mechanism driving a correlated pattern of evolution. We examine the proportionality between genetic variance and patterns of trait evolution in a system whose developmental processes are well understood to gain insight into how such alignment between morphological divergence and genetic variation might be maintained over macroevolutionary time. Primate molars present a model system by which to link developmental processes to evolutionary dynamics because of the biased pattern of variation that results from the developmental architecture regulating their formation. We consider how this biased variation is expressed at the population level, and how it manifests through evolution across primates. There is a strong correspondence between the macroevolutionary rates of primate molar divergence and their genetic variation. This suggests a model of evolution in which selection is closely aligned with the direction of genetic variance, phenotypic variance, and the underlying developmental architecture of anatomical traits.