The bay scallop and Peruvian scallop are economically important species. Interspecific hybrids of these two scallops outperformed both of their parent species in multiple growth traits but exhibited decreased fertility, which provides good models for the study of heterosis and species divergence. Genetic mapping serves as a chromosomal-level framework to investigate the molecular mechanisms of hybridization and introgression. In this study, high-resolution linkage maps were constructed for the bay and Peruvian scallops with an interspecific hybrid family. The linkage map of the bay scallop covered over 98.9% of the whole genome with 2994 mapped markers and the average marker interval of 0.32 cM. For the Peruvian scallop, 1585 markers were mapped with the average maker interval of 0.51 cM, covering 97.7% of the genome. Both the two linkage maps have 16 linkage groups, corresponding to the haploid chromosome number of the two species. Approximately, 54.5% of markers exhibited significant deviation from the expected Mendelian ratio of segregation, lending insights into the intrinsic incompatibility between the two species. QTLs related to growth and shell coloration were detected, which could explain 13.1% and 74.9% of the phenotypic variance, respectively. This represents important information for further evaluation. These findings are an important addition to the genomic resources for scallop genetic studies, and are especially useful for investigations on genomic incompatibility for hybridization, genome evolution of closely related species, and genetic enhancement programs in aquaculture.