Genetic diversity is a fundamental component of biodiversity. Examination of global patterns of genetic diversity can help highlight mechanisms underlying species diversity, though patterns may differ across the genome. Here, we compiled 6862 observations of genetic diversity from 492 species of marine fish, assessed their associations with macroecological drivers, and tested among hypotheses for diversity gradients: the founder effect hypothesis, the kinetic energy hypothesis, and the productivity-diversity hypothesis. We found that mitochondrial genetic diversity followed geographic 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 global patterns. Despite these differences, all genetic diversity metrics were strongly correlated with chlorophyll-a concentration, while mitochondrial diversity was also positively associated with sea surface temperature. Our results provide support for the kinetic energy hypothesis, which predicts that elevated mutation rates at higher temperatures increase mitochondrial diversity, and the productivity-diversity hypothesis, which posits that resource-rich regions support larger populations with greater genetic diversity. Overall, these findings reveal how environmental variables can influence mutation rates and drift in the ocean, caution against using mitochondrial macrogenetic patterns as proxies for nuclear DNA, and aid in defining global gradients of genetic diversity.