Genetic diversity is a fundamental component of biodiversity and the medium for speciation events. Examination of global patterns of genetic diversity can help highlight mechanisms underlying species diversity. Here, we compiled 6862 observations of genetic diversity from 492 species of marine fish globally, assessed their associations with macroecological drivers, and tested among three hypotheses for diversity gradients: the founder effect hypothesis, the kinetic energy hypothesis, and the productivity-richness hypothesis. We found that mitochondrial genetic diversity follows latitudinal and longitudinal gradients similar to those of species diversity, being highest near the equator, particularly in the Coral Triangle, while nuclear genetic diversity did not follow clear geographic patterns. Despite these differences, all genetic diversity metrics were positively correlated with chlorophyll, while mitochondrial diversity was also positively associated with sea surface temperature. These findings provide support for the kinetic energy hypothesis, which predicts that elevated metabolic and mutation rates at higher temperatures should increase mitochondrial diversity, and the productivity-richness hypothesis, which posits that resource-rich regions support larger populations with greater genetic diversity. Overall, these findings reveal how environmental controls on mutation and drift in the ocean combine to establish global gradients of genetic diversity within species, and in turn, community assemblages.