Wolbachia popcorn (wMelPop), a life-shortening strain of Wolbachia, has been proposed as an agent for suppressing transmission of dengue fever following infection of the vectoring mosquito Aedes aegypti. However, evolutionary changes in the host and Wolbachia genomes might attenuate any life span effects mediated by wMelPop. Here we test for attenuation by selecting strains of Drosophila melanogaster infected with wMelPop for early and late reproduction in three independent outcrossed populations. Selection caused divergence among the lines in longevity. This divergence was mostly associated with the host genetic background rather than the Wolbachia infection, although there were also interactions between the host and Wolbachia genomes. Development time, viability, and productivity were not altered by selection. The implications of these results are discussed in light of the intended use of wMelPop for suppressing disease transmission.