Wolbachia are obligate, intracellular bacterial symbionts of insects that have been proven to reduce transmission of viral diseases from insects to humans. Transfection of Wolbachia into the dengue mosquito, Aedes aegypti, has successfully reduced dengue transmission in 11 countries1. Wolbachia induces physiological changes in its hosts, but the mechanistic basis and the metabolic contributions to these host-symbiont interactions are unresolved. The Wolbachia genome lacks vital metabolism genes, suggesting the symbiont scavenges resources from its host. We employed 1H NMR-based metabolomics and targeted UPLC metabolite quantification to identify Wolbachia-induced metabolic changes. We investigated the infection of two strains, wMel and wMelPop, at two diet levels. The effects of diet overpower the metabolic changes attributed to wMel but did suggest that wMel participates in minor metabolic provisioning to Ae. aegypti. Conversely, wMelPop triggered immune system pathways including melanogenesis and reactive oxygen generation and management. Furthermore, increased levels of amino acids in wMelPop infected mosquitos suggests that altered nitrogen metabolism is a key effect of the infection. Our research supports the conclusion that wMelPop is the more aggressive strain and triggers the immune response in Ae. aegypti, potential limiting wMelPop’s ability to sustain infection in the field. In contrast, wMel is more benign to the host and thus more likely to form a stable inheritable infection. The strains wMel and wMelPop occupy distinct positions on the spectrum of mutualistic-parasitic symbiotic relationships that Wolbachia can exhibit.