Various hypotheses for the peopling of the Japanese archipelago have been proposed, which can be classified into three models: transformation, replacement, and hybridization. In recent years, one of the hybridization models ("dual-structure model") has been widely accepted. According to this model, Neolithic hunter-gatherers known as Jomon, who are assumed to have originated in southeast Asia and lived in the Japanese archipelago greater than 10,000 years ago, admixed with an agricultural people known as Yayoi, whom were migrants from the East Asian continent 2,000–3,000 years ago. Meanwhile, some anthropologists propose that rather, morphological differences between the Jomon and Yayoi people can be explained by microevolution following the lifestyle change. To resolve this controversy, we compared three demographic models by approximate Bayesian computation using genome-wide single nucleotide polymorphism (gwSNP) data from the Ainu people who are thought to be direct descendants of indigenous Jomon. If we assume Chinese people sampled in Beijing from HapMap have the same ancestry as Yayoi, then the hybridization model is predicted to be between 29 and 63 times more likely than the replacement and transformation models, respectively. Furthermore, our data provide strong support for a model in which the Jomon lineages had population structure diversified in local areas before the admixture event. Initial divergence between the Jomon and Yayoi ancestries was dated to late Pleistocene, followed by the divergence of Jomon lineages at early Holocene. These results suggest gwSNP data provides a detailed picture of the complex hybridization model for Japanese population history.