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The freshwater pearl mussel Margaritifera margaritifera is an ecologically important globally endangered species, yet little is known about its biodiversity and population genetics in North American populations. This study focused on M. margaritifera from six locations within two stream systems in central and eastern Massachusetts, USA, to understand the historical impact of damming and habitat fragmentation on local population structure and genetic diversity.Approximately 300 informative single nucleotide polymorphisms were generated from 59 individuals across six geographical locations, using the restriction‐site‐associated DNA sequencing approach. Genotypes were also gleaned from publicly available RNA sequencing data of 23 French M. margaritifera samples.Predictions of population structure using discriminant analysis of principal components and fastStructure both indicate the existence of a single genetic population in central and eastern Massachusetts, and a clear separation from French individuals. This observation is further supported by frequency‐based calculations of population genetics, which indicate near‐complete admixture and a high number of migrants between Massachusetts sites.These results suggest that the effects of habitat fragmentation from damming in the past century have not radiated through the Massachusetts population of M. margaritifera, potentially because of the long lifespan and generation time of the species. However, the Massachusetts population has similar levels of genetic diversity to the endangered populations in Europe, and these factors should be considered by conservationists when creating conservation and management plans.The findings of this study suggest that populations in North America are reasonably healthy and diverse and that, as one population, the study area represents one conservation unit. This indicates that dam removal, habitat restoration, and captive breeding programmes may be viable options to increase the small population numbers and retain a substantial portion of genetic diversity without sacrificing local adaptation. [ABSTRACT FROM AUTHOR]