The commercially important Atlantic surfclam, Spisula solidissima solidissima was recently discovered to be in sympatry with its cryptic sister taxon, the “southern” Atlantic surfclam S.s. similis, nearshore in southern New England. The extent of hybridization between the two nominal subspecies in sympatry and the population structure of each taxon within New England may have major impact on the fisheries productivity. This study uses ddRAD sequencing conducted on over 400 samples to analyze population structure, genomic diversity, and gene flow patterns within and between these two nominal subspecies. After accounting for high genealogical diversity associated with uniformly large effective population sizes, genomic results supported previous studies showing species-level separation between S.s. similis and S.s. solidissima. The genomic data identified, for the first time, morphologically cryptic, deep population structure within S.s. solidissima. One operational taxonomic unit (OTU) was found only at inshore sites south of Cape Cod. The other OTU was found both inshore offshore, and was the only OTU on the commercially fished Atlantic continental shelf. No indication of hybridization was detected between S.s. similis and S.s. solidissima, but a small number of hybrids between the two S.s. solidissima OTUs showed various levels of admixture. Within S.s. similis, similar levels of genomic diversity were found in southern New England and Georgia populations, and population structure patterns were roughly consistent with equilibrium isolation by distance gene flow. With a few exceptions, moderate gene flow roughly consistent with isolation by distance was also inferred among populations from each S.s. solidissima OTU. With management of the commercial fishery challenged by population responses to climate change and interest growing in surfclam aquaculture, understanding population connectivity and the distribution of genetic diversity in these taxa can help adaptively manage surfclam resources. The implications of these population structure patterns for surfclam fisheries management are discussed.