The Amazon–Orinoco plume (AOP) is the world’s largest freshwater and sediment discharge into the ocean. Previous studies limited to mtDNA suggest that the swimming crab Callinectes ornatus Ordway, 1863 exists as two distinct genetic clusters separated by the AOP. However, questions concerning migration, diversification time, and species delimitation are unresolved. Densely sampling markers across the genome (SNPs) could elucidate the evolutionary processes within this species. Here, we combined mtDNA data and ddRAD-seq to explore the diversification patterns and processes within the swimming crab C. ornatus. We show great genetic differentiation between groups on the north and south sides of the plume but also signs of hybridization. Demographic modeling indicates the divergence between groups starting around 8 Mya following the AOP’s formation. After a period of isolation, we detect two incidences of secondary contact with stronger migration in concordance with the North Brazil Current flow. Our results suggest speciation with gene flow explained by the interplay among the AOP, oceanographic currents, and long larval dispersal. This work represents the first investigation employing ddRAD-seq in a marine invertebrate species with distribution encompassing the north and south Atlantic and sheds light on the role of the AOP in the diversification of a marine species.