Widespread dispersal of progeny is expected to result in enough gene flow to maintain genetic homogeneity over large areas. Surveys of genetic markers in species with planktonic larvae have mostly confirmed this expectation. However, genetic structure has occasionally been found at small spatiotemporal scales and interpreted as evidence of restricted dispersal, natal homing, sweepstakes reproductive success, or natural selection. We investigated genetic population structure in blue crabs from the Atlantic and Gulf of Mexico coasts of North America. Sampling was most intensive from five estuaries along the coast of Louisiana, with megalopae, juveniles and adults sampled from 2010 to 2016. 1446 individuals were genotyped at 2486 SNPs in 1363 putative protein-coding loci. Levels of differentiation between locations were consistently low, but significant differentiation was found among locations and among years. No evidence was found for chaotic genetic patchiness or sweepstakes reproductive success: no genetic differentiation was detected among collections of megalopae and none of the sampled individuals were closely related. Our results indicate that gene flow in blue crabs maintains near genetic homogeneity from the northern Gulf of Mexico through the Atlantic coast of North America.