The Black Skimmer (Rynchops niger) is a charismatic representative of coastal-nesting waterbird communities in North America and freshwater riverine and coastal systems in South America. Skimmers are at high risk of decline due to threats including habitat loss, human activity, and climate change throughout the annual cycle. To understand range-wide population connectivity, eight microsatellite loci were used to reveal genetic differentiation between North American Pacific and Atlantic Coasts, including the Gulf of Mexico, and very strong differentiation between the North American sites and a site in Peru, South America. A reduced dataset, incorporating previously published data from South America, documented strong inter-continental differentiation and moderate differentiation among sites within South America in a pattern inconsistent with current subspecies designations, and suggesting a more complex pattern of dispersal. We recommend combined use of telemetry and genomic tools to assist in future delineation of skimmer subspecies ranges and non-breeding habitat use in South America. Because genetic diversity was relatively low in North America and higher in South America, genetics could determine whether skimmers in South America represent the ancestral population now expanding along the Atlantic and Pacific Coasts of North America. Detailed knowledge of seasonal movement and non-breeding habitat use that can be obtained by telemetry and population-wide molecular analyses will be essential to informing effective management across the Americas.