The degree of connectivity among populations influences their ability to respond to natural and anthropogenic stressors. In marine systems, determining the scale, rate, and directionality of larval dispersal is therefore, central to understanding how coral metapopulations are interconnected and the degree of resiliency in the event of a localized disturbance. Understanding these source-sink dynamics is essential to guide restoration efforts and for the study of ecology and evolution in the ocean. The patterns and mechanisms of connectivity in the deep-sea (>200 m deep) are largely understudied. In this study, we investigated the spatial diversity patterns and metapopulation connectivity of the octocoral Paramuricea biscaya throughout the northern Gulf of Mexico (GoM). Paramuricea biscaya is one of the most abundant corals on the lower continental slope (between 1,200 and 2,500 m) in the GoM. The 2010 Deepwater Horizon oil spill (DWH) directly impacted populations of this species and thus are considered primary targets for restoration. We used a combination of seascape genomic analyses, high-resolution ocean circulation modeling, and larval dispersal simulations to quantify the degree of population structuring and connectivity among P. biscaya populations. Evidence supports the hypotheses that the genetic diversity of P. biscaya is structured by depth, and that larval dispersal among connected populations is asymmetric due to dominant ocean circulation patterns. Our results suggest that there are intermediate unsampled populations in the central GoM that serve as stepping stones for dispersal. The data suggest that the DeSoto Canyon area, and possibly the West Florida Escarpment, critically act as sources of larvae for areas impacted by the DWH oil spill in the Mississippi Canyon. This work illustrates that the management of deep-sea marine protected areas should incorporate knowledge of connectivity networks and depth-dependent processes throughout the water column.