The eastern oyster (Crassostrea virginica) is an ecologically and economically valuable species along the East Coast of the United States and within the Gulf of Mexico. However, the oyster fishery is being threatened by anthropogenic and environmental stressors such as salinity and temperature fluctuations and increased fishing pressure, and an improved understanding of genetic differentiation is vital for future management of C. virginica. In addition, the use of low-cost genotyping in oyster breeding programs is increasing. A microhaplotype-based genotyping panel utilizing genotyping-in-thousands by sequencing (GT-seq) technology was previously developed using individuals from Gulf of Mexico and East Coast populations. While this panel successfully captures patterns of genetic variation across the C. virginica range, the high degree of genetic diversity and prevalence of null alleles in mollusc genomes pose challenges to effective use of the panel, particularly in achieving accurate genotype calling. Here, we report on the progress of improving genotyping accuracy through additional optimization of the microhaplotype panel using information from pair crosses. Validation of the panel’s ability to accurately determine pedigree relationships and differentiate populations will also be presented. Broader applications for aquaculture, restoration, and fisheries management will be discussed, highlighting the potential impact of this genotyping panel on the future of oyster fisheries management and selective breeding.