Approximately a quarter of eukaryotes are infected with the bacterium Wolbachia. Its broad success as a vertically transmitted infection has been historically difficult to explain given the myriad of parasitic impacts characterized across Wolbachia's host range. Using the Drosophila model and their natively associated Wolbachia, we show that Wolbachia infection supports fly development and buffers against nutritional stress. Wolbachia infection across several fly genotypes and a range of nutrient conditions resulted in reduced pupal mortality, increased adult emergence, and larger size. We determined that the exogenous supplementation of pyrimidines rescued these phenotypes in the Wolbachia-free, flies suggesting that Wolbachia plays a role in providing this metabolite that is normally limiting for insect growth. Additionally, Wolbachia was sensitive to host pyrimidine metabolism: Wolbachia titers increased upon transgenic knockdown of the Drosophila de novo pyrimidine synthesis pathway but not knockdown of the de novo purine synthesis pathway. We propose that Wolbachia acts as a nutritional symbiont to supplement insect development and increase host fitness: a selective advantage that could contribute to its high frequency in nature.