Viral diseases can change plant metabolism, with potential impacts on the quality of the plant’s food supply for insect pests, including virus vectors. The banana aphid, Pentalonia nigronervosa Coquerel, is the vector of the Banana bunchy top virus (BBTV), the causal agent of Banana bunchy top disease (BBTD), the most devastating viral disease of bananas in the world. The effect of BBTV on the life-history traits and population dynamics of P. nigronervosa remains poorly understood. We therefore studied the survival rate, longevity, daily fecundity per aphid, tibia length, population growth, and winged morph production of a P. nigronervosa clone grown on healthy or infected, dessert, or plantain banana plants. We found that daily fecundity was higher on infected banana than on healthy banana plants (plantain and dessert), and on plantain than on dessert banana plants (healthy and infected). Survival and longevity were lower on infected dessert bananas than on other types of bananas. In addition, virus infection resulted in a decrease in aphid hind tibia length on both plant genotypes. The survival and fecundity table revealed that the aphid net reproduction rate (Ro) was highest on plantains (especially infected plantain), and the intrinsic growth rate (r) was highest on infected plants. Finally, the increase of aphids and alate production was faster first on infected plantain, then on healthy plantain, and lower on dessert banana (infected and uninfected). Our results reinforce the idea of indirect and plant genotype-dependent manipulation of P. nigronervosa by the BBTV.