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Microsporidia are spore-forming intracellular parasites of various invertebrates and vertebrates. <i>Vairimorpha bombi</i> negatively affects the fitness of bumblebees and its prevalence correlates with declining bumblebee populations. The invasive alien species <i>Bombus terrestris</i> colonized Japan and possibly introduced new parasites. To assess the infection prevalence of <i>V. bombi</i> in Japanese bumblebees and <i>B. terrestris</i>, we investigated <i>V. bombi</i> infections using PCR and microscopy. The prevalence of sporulating <i>V. bombi</i> infections in three <i>Bombus</i> s. str. species/subspecies was low, whereas that of non/low-sporulating <i>Vairimorpha</i> sp. infections in three <i>Diversobombus</i> species/subspecies was high. Invasive <i>B. terrestris</i> showed low prevalence of non/low-sporulating <i>V. bombi</i> infections and shared the same <i>V. bombi</i> haplotype with <i>B. hypocrita</i> found in Hokkaido, where <i>B. terrestris</i> is present, and in Honshu, where <i>B. terrestris</i> is absent. Although <i>V. bombi</i> may have been introduced with <i>B. terrestris</i> colonies imported from Europe, it seems to be originally distributed in Japan. Furthermore, a new <i>Vairimorpha</i> sp. was found in Japanese bumblebee species. <i>V. bombi</i> and <i>Vairimorpha</i> sp. showed different organ and host specificities in bumblebees. There are no reports on the specific effects of other <i>Vairimorpha</i> spp. on bumblebees; further studies are needed to clarify the individual characteristics of <i>Vairimorpha</i> spp.