Aim The genus Camellia is widely distributed, primarily in East Asia. Camellia japonica is located at the northern limit of this genus distribution, and elucidating its distribution changes is crucial for understanding the evolution of plants in this region, as well as their relationship with geological history and climate change. Also, the classification of sect. Camellia in Japan has not been clarified. Therefore, the aim of this study is to understand the evolutionary history of Japanese sect. Camellia. Location Japan, Korea, Taiwan, and the coastal area of China Taxon Camella (Theaceae). Methods The genetic population structure was analyzed by SNP data using MIG-seq. The relationship between Japanese sect. Camellia including the related species in China was further inferred from the phylogeny generated by RA x ML, SplitsTree and PCA. Population genetic structure was inferred using a Bayesian clustering method (ADMIXTURE). We then employed approximate Bayesian computation to explore the changes in population, asking which events best explain the phylogeographical signature. Ecological niche modeling was combined with genetic analyses to compare current and past distributions. Results The analyses consistently showed that C. japonica and C. rusticana are distinct, having diverged from each other between approximately 5.4 and 12 million years ago. Furthermore, C. japonica differentiated into four major populations (North, South, Ryukyu-Taiwan, and Continent). Main Conclusion Japanese sect. Camellia underwent speciation during archipelago formation, reflecting its ancient evolutionary history compared with other native Japanese plants. The conventional hypothesis that C. rusticana diverged from C. japonica in snow-rich environments under Quaternary period was rejected. Our results suggest that both species have been independent since ancient times, and that ancestral populations of C. japonica have persisted in northern regions. Furthermore, it is estimated that C. japonica population on the continent experienced a back-dispersal event from southern Japan during the late Pleistocene glaciation.