Extreme environmental gradients represent excellent study systems to better understand the variables that mediate patterns of genomic variation between populations. They also allow for more accurate predictions of how future environmental change might affect marine species. The Persian/Arabian Gulf is extreme in both temperature and salinity while the adjacent Gulf of Oman has conditions more typical of tropical oceans. The sea urchin Echinometra sp. EZ inhabits both of these seas and plays a critical role in coral reef health as a grazer and bioeroder, but, to date, there have been no population genomic studies on this or any urchin species in this unique region. E. sp. EZ's life history traits (e.g., large population sizes, large reproductive clutches, and long life spans), in theory, should homogenize populations unless non-neutral processes are occurring. Here, we generated a draft genome and a restriction-site associated DNA sequencing dataset from seven populations along an environmental gradient across the Persian/Arabian Gulf and the Gulf of Oman. The estimated genome size of E. sp. EZ was 609 Mb and the heterozygosity was amongst the highest recorded for an echinoderm at 4.5%. We recovered 918 high quality SNPs from 85 individuals which we then used in downstream analyses. Population structure analyses revealed a high degree of admixture between all sites, although there was population differentiation and significant pairwise FST values between the two seas. Preliminary results suggest migration is bidirectional between the seas and nine candidate loci were identified as being under putative natural selection, including one collagen gene. This study is the first to investigate the population genomics of a sea urchin from this extreme environmental gradient and is an important contribution to our understanding of the complex spatial patterns that drive genomic divergence.