We previously revealed the presence of six genetically distinct matrilineal populations of the Japanese dormouse Glirulus japonicus in the distribution range of Honshu, Shikoku, and Kyushu islands. In this study, we extended this analysis using mitochondrial cytochrome b gene sequences (n = 96) and Y-chromosome-specific SRY gene sequences (n = 22) from individuals collected from Honshu, Shikoku, Kyushu, and Oki Dogo I. The cytochrome b sequence data allowed us to define precise geographic ranges of the six previously known and three newly found distinct matrilineal lineages: northeastern Honshu (I), east-central Honshu (II), west-central Honshu and the Kii Peninsula (III), the western part of Honshu (IV), Shikoku (V), westernmost Honshu and Kyushu (VI), the northern part of central Honshu (VII), the southern part of central Honshu (VIII), and Oki Dogo I. (IX). Our inference of geographic borders suggests that regions of lower and higher altitudes in the mountain systems played important roles in driving the hosting and separation of lineages, respectively. Six matrilineal lineages (I, II, V, VI, VIII, and XI) were shown to possess their own SRY haplotypes, while lineages III and IV shared one haplotype. These data together with our previous observation of nuclear ribosomal RNA gene variation indicate advanced populational subdivision in this species. It is thus evident that each of the populations, including those living at high latitudes and in limited geographic spaces, have survived for several million years. A specific ability to tolerate cold may have permitted G. japonicus to preserve anciently diverged lineages in each locality.