Species boundaries and population structure within the anthozoan sub-class Octocorallia have been obfuscated due to insufficient differences in the morphological characters and molecular markers traditionally used to distinguish between closely related taxa. NGS methods provide unprecedented genomic resources that show promise in resolving octocoral taxonomies. Target enrichment of Ultraconserved Elements (UCEs) has been successful at resolving deep phylogenetic relationships within Octocorallia. To evaluate the utility of UCEs in resolving species boundaries and identifying admixture among octocoral populations, UCEs were sequenced from 64 Mediterranean and North Atlantic octocorals in the genus Alcyonium. The species boundaries among these octocorals have been corroborated across studies that used morphological, reproductive and genetic markers. 32 of these individuals represented four geographically distinct populations of the species A. coralloides. Using 2,921 recovered UCE loci, we built a highly-supported phylogenetic tree that largely resolved monophyletic clades for the putative Alcyonium species and A. coralloides populations. Within each of three clades, single nucleotide polymorphisms (SNPs) were called and used to perform Discriminant Analysis of Principal Components (DAPC) and STRUCTURE analyses. The DAPC and STRUCTURE analyses designated species that were congruent with putative species boundaries and separated A. coralloides individuals into populations. These analyses support that UCEs show promise as markers to resolve not only deep, but also shallow-level relationships among octocorals.