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Interactions between environmental factors and complex life‐history characteristics of marine organisms produce the genetic diversity and structure observed within species. Our main goal was to test for genetic differentiation among eastern oyster populations from the coastal region of Canadian Maritimes against expected genetic homogeneity caused by historical events, taking into account spatial and environmental (temperature, salinity, turbidity) variation. This was achieved by genotyping 486 individuals originating from 13 locations using RADSeq. A total of 11,321 filtered SNPs were used in a combination of population genomics and environmental association analyses. We revealed significant neutral genetic differentiation (mean FST = 0.009) between sampling locations, and the occurrence of six major genetic clusters within the studied system. Redundancy analyses (RDAs) revealed that spatial and environmental variables explained 3.1% and 4.9% of the neutral genetic variation and 38.6% and 12.2% of the putatively adaptive genetic variation, respectively. These results indicate that these environmental factors play a role in the distribution of both neutral and putatively adaptive genetic diversity in the system. Moreover, polygenic selection was suggested by genotype–environment association analysis and significant correlations between additive polygenic scores and temperature and salinity. We discuss our results in the context of their conservation and management implications for the eastern oyster. [ABSTRACT FROM AUTHOR]