The complex genomic features of oysters shape inter-individual and intra-individual haplotype diversity, which is expected to be the basis for allele-specific expression (ASE). Through identifying and comparing ASEGs in different tissues of multiple oyster individuals from the same natural population, we demonstrate that the occurrence of ASEGs is more likely due to random haplotype divergence during the evolutionary process of oysters, rather than being driven by directional selection. Further exploration of the relationship between genetic divergence among individuals and the occurrence of ASE revealed that conserved ASEGs tend to undergo parallel evolution among individuals.