Species in the genus play important roles for people's food and nutrition especially and . To understand their evolutionary history, genome structure, and population-level genetic variation, we performed a high-quality genome sequencing of and the corresponding comparative genomic analysis. The genome size of was similar to , but 1.5 times larger than that of . Several factors were responsible for genome size variation including gene numbers, repetitive elements, and gene lengths. Phylogenomic analysis revealed that the estimated divergence time between and other is ∼79.1 million years ago (Mya), while the divergence between and occurred in ∼54.8 Mya. Population genomic analysis also provided insight into the demographic history of and , indicating that their populations fluctuated over time with global climate change during Marine Isotope Stage 5-2. Moreover, despite the highly similar external morphologies of and , their genomic properties were remarkably different. The genome only shared 14% homologous syntenic blocks with and possessed more genes encoding carbohydrate-active enzymes and secondary metabolite biosynthesis proteins. The cross-taxa transferability rates of simple sequence repeat (SSR) and insertion or deletion (InDel) markers within the genus were also lower than that previously observed for species within the same genus. Taken together, these results indicate a high level of genetic differentiation between these two species. Consequently, our study provides new insights into the genomic evolution and genetic differentiation of species that will facilitate future genetic breeding.