Maternally inherited Wolbachia endosymbionts manipulate arthropod reproduction in various ways. In the butterfly Eurema mandarina, a cytoplasmic incompatibility-inducing Wolbachia strain wCI and the associated mtDNA haplotypes are known to originate from the sister species Eurema hecabe, which offered a good case study for microbe-mediated hybrid introgression. Besides wCI, some females with the Z0 karyotype harbour a distinct Wolbachia strain wFem, which causes all-female production by meiotic drive and feminization. We report that a considerable proportion of E. mandarina females (65.7%) were infected with both wCI and wFem (CF) on Tanegashima Island. While females singly infected with wCI (C) produced offspring at a 1 : 1 sex ratio, CF females produced only females. Although Z-linked sequence polymorphism showed no signs of divergence between C and CF females, mtDNA split into two discrete clades; one consisted of C females and the other CF females, both of which formed a clade with E. hecabe but not with uninfected E. mandarina. This suggests that CF matrilines also, but independently, experienced a selective sweep after hybrid introgression from E. hecabe. Distinct evolutionary forces were suggested to have caused C and CF matrilines to diverge, which would be irreversible because of the particular phenotype of wFem.