Understanding how genomic architecture and demographic history interact to shape patterns of genomic divergence is central to explaining adaptive radiation and speciation. Here, we provide the first full sequence patterns of diversity and differentiation for Hydrophis sea snakes, using population sampling of three ecomorphologically distinct, coexisting species that diverged near-simultaneously within the last few million years (H. major, H. elegans and H. curtus). We found recent population expansions in all three species, with little evidence for pervasive interspecific gene flow. Genomic landscapes of differentiation were correlated across pairwise comparisons, with relative divergence associated with local reductions in nucleotide diversity but mostly decoupled from absolute divergence. Peaks of differentiation were concentrated in putative pericentromeric regions, consistent with linked selection in shared low-recombination regions. In contrast, a large region of low relative differentiation on chromosome 2 showed elevated diversity across all species and overlapped a prominent cluster of chemosensory vomeronasal type-2 receptor (V2R) genes. Overall, our results suggest that shared demographic history and linked selection shape a common genomic landscape in Hydrophis, while chemosensory receptor gene evolution may have contributed to ecological diversification during the land-to-sea transition of these unique marine reptiles.