While population declines can drive the loss of genetic diversity under some circumstances, it has been unclear whether this loss is a general consequence of overharvest in highly abundant marine fishes. Here, we use a phylogenetic approach across 160 species and 11,658 loci to show that allelic richness was on average 11% lower (p < 0.0001) in overharvested populations, even after accounting for the effects of body size, latitude, and other factors. Heterozygosity was 2% lower (p = 0.030). Simulations confirmed that these patterns are consistent with a recent bottleneck in abundant species and also showed that our analysis likely underestimates the loss of rare alleles by a factor of two or three. This evidence suggests that overharvest drives the decay of genetic diversity across a wide range of marine fishes. Such reductions of genetic diversity in some of the world’s most abundant species may lead to a long-term impact of fishing on their evolutionary potential, particularly if abundance remains low and diversity continues to decay.