Abstract Background The Portuguese oyster Crassostrea angulata and the Pacific oyster C. gigas are two major Crassostrea species that are naturally distributed along the Northwest Pacific coast and possess great ecological and economic value. Here, we report the construction and comparative analysis of the chromosome-level haplotype-resolved genomes of the two oyster congeners. Findings Based on a trio-binning strategy, the PacBio high-fidelity and Illumina Hi-C reads of the offspring of the hybrid cross C. angulata (♂) × C. gigas (♀) were partitioned and independently assembled to construct two chromosome-level fully phased genomes. The assembly size (contig N50 size, BUSCO completeness) of the two genomes were 582.4 M (12.8 M, 99.1%) and 606.4 M (5.46 M, 98.9%) for C. angulata and C. gigas, respectively, ranking at the top of mollusk genomes with high contiguity and integrity. The general features of the two genomes were highly similar, and 15,475 highly conserved ortholog gene pairs shared identical gene structures and similar genomic locations. Highly similar sequences can be primarily identified in the coding regions, whereas most noncoding regions and introns of genes in the same ortholog group contain substantial small genomic and/or structural variations. Based on population resequencing analysis, a total of 2,756 species-specific single-nucleotide polymorphisms and 1,088 genes possibly under selection were identified. Conclusions This is the first report of trio-binned fully phased chromosome-level genomes in marine invertebrates. The study provides fundamental resources for the research on mollusk genetics, comparative genomics, and molecular evolution.