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Abstract Obovaria olivariais a species of freshwater mussel native to the Mississippi River and Laurentian Great Lakes‐St. Lawrence River drainages of North America. This mussel has experienced population declines across large parts of its distribution and is imperiled in many jurisdictions.Obovaria olivariauses the similarly imperiledAcipenser fulvescens(Lake Sturgeon) as a host for its glochidia. We employed mitochondrial DNA sequencing and restriction site‐associated DNA sequencing (RAD‐seq) to assess patterns of genetic diversity and population structure ofO. olivariafrom 19 collection locations including the St. Lawrence River drainage, the Great Lakes drainage, the Upper Mississippi River drainage, the Ohioan River drainage, and the Mississippi Embayment. Heterozygosity was highest in Upper Mississippi and Great Lakes populations, followed by a reduction in diversity and relative effective population size in the St. Lawrence populations. PairwiseF_STranged from 0.00 to 0.20, and analyses of genetic structure revealed two major ancestral populations, one including all St. Lawrence River/Ottawa River sites and the other including remaining sites; however, significant admixture and isolation by river distance across the range were evident. The genetic diversity and structure ofO. olivariais consistent with the existing literature onAcipenser fulvescensand suggests that, although northern and southernO. olivariapopulations are genetically distinct, genetic structure inO. olivariais largely clinal rather than discrete across its range. Conservation and restoration efforts ofO. olivariashould prioritize the maintenance and restoration of locations whereO. olivariaremain, especially in northern rivers, and to ensure connectivity that will facilitate dispersal ofAcipenser fulvescensand movement of encysted glochidia.