The invasive orange spiny whitefly (OSW) Aleurocanthus spiniferus has extended its distribution to non-native areas since the early 20th century. In a similar manner, the invasive tea spiny whitefly (TSW) A. camelliae has been expanding over East Asia in recent decades. In this study, the genetic diversity of OSW and TSW and of their important parasitoid wasp Encarsia smithi was investigated in China and Japan to enable more efficient biological control policies. We detected two phylogenetic groups (haplogroups A1 and A2) in OSW and three phylogenetic groups (haplotypes B1 and B2, and haplogroup B3) in TSW in China; however, only a single haplotype was detected in each whitefly species in Japan. Based on historical records and molecular data, OSW was considered to be native to China whereas TSW has probably expanded to China from a more southern location in the last 50 years; China appears to be the source region for OSW and TSW invading Japan. In E. smithi, two phylogenetic groups were detected in Japan: haplotype I, associated with OSW, and haplogroup II mostly associated with TSW, except in two locations. These data support the hypothesis that E. smithi parasitizing TSW in Japan did not originate from the existent population parasitizing OSW but was newly imported into Japan following the invasion of its host.