Understanding patterns of population connectivity is fundamental for effective conservation and restoration of vulnerable marine resources. Determining gene flow rates and directions is particularly important for determining sources and sinks of populations and thus the resiliency or susceptibility of populations to disturbances. This can be challenging for deepwater foundation species, particularly those that are sessile as adults that live in distinct patches; only connected across spatial scales by their pelagic larvae. Thus, we used genomic approaches, including restriction-site-associated sequencing (RADSeq) and target-capture genomics, to ascertain 1000s of single nucleotide polymorphisms (SNPS) in benthic invertebrates, including deep-water corals and cold-seep mussels along the U.S. eastern seaboard and gulf coasts.  Using genomics, we reveal complex patterns in connectivity while elucidating evolutionary processes that drive population differentiation. We show that differentiation across a gradient in depth is a common trend, and support that diversification occurs in an onshore to offshore direction. Our analyses go beyond connectivity patterns to elucidate genes important in adaptation to deep-sea environments. Taken together, results from genomic approaches can help in conservation decision-making, providing resource managers suggestions on ideal places for restoration and conservation— activities that are particularly important in the U.S. Gulf of Mexico region.