The aphid Ceratovacuna nekoashi and its allied species have been a taxonomically difficult group. They form peculiar “cat's-paw” galls (called “Nekoashi” in Japanese) on Styrax trees and also use Microstegium grasses as their secondary hosts. Through sampling aphids from both Styrax galls and Microstegium grasses in South Korea, Japan and Taiwan, and sequencing their DNA, we made it clear that four distinct species occur in these regions: C. nekoashi (Sasaki), C. oplismeni (Takahashi), C. orientalis (Takahashi) and C. subtropicana sp. nov. In Korea, C. nekoashi forms galls on both S. japonicus and S. obassia, whereas in Japan the species forms galls on the former but not on the latter; our molecular analyses unequivocally indicated the occurrence of a single species in South Korea and mainland Japan. Aphids of the four species on the secondary host were morphologically discriminated from one another. The identity of the primary- and secondary-host generations was also clarified for each species. All four species were found to produce second-instar sterile soldiers in their Styrax galls, and first-instar soldiers were found in colonies of C. subtropicana on the secondary host.