Striped Bass, Morone saxatilis (Walbaum, 1792), is an anadromous fish species that supports fisheries throughout North America and is native to the North American Atlantic Coast. Due to long coastal migrations that span multiple jurisdictions, a detailed understanding of population genomics is required to untangle demographic patterns, understand local adaptation, and characterize population movements. This study used 1,256 single nucleotide polymorphism (SNP) loci to investigate genetic structure of 477 Striped Bass sampled from 15 locations spanning the North American Atlantic coast from the Gulf of St. Lawrence, Canada, to the Cape Fear River, United States. We found striking differences in neutral divergence among Canadian sites, which were isolated from each other and US populations, compared with US populations that were much less isolated. Our SNP dataset was able to assign 99% of Striped Bass back to six reporting groups, a 39% improvement over previous genetic markers. Using this method, we found (a) evidence of admixture within Saint John River, indicating that migrants from the United States and from Shubenacadie River occasionally spawn in the Saint John River; (b) Striped Bass collected in the Mira River, Cape Breton, Canada, were found to be of both Miramichi River and US origin; (c) juveniles in the newly restored Kennebec River population had small and nonsignificant differences from the Hudson River; and (d) tributaries within the Chesapeake Bay showed a mixture of homogeny and small differences among each other. This study introduces new hypotheses about the dynamic zoogeography of Striped Bass at its northern range and has important implications for the local and international management of this species.