Viewing interspecies relationships through the lens of bioenergetics enables a flexible conceptual framework to understand why virulence is context-dependent in arthropod-borne diseases. Here, we engineered a system of metabolic interdependence in Ixodes scapularis where nutrients were allocated according to the glycolytic or oxidative phosphorylation cellular state. The rickettsial agent Anaplasma phagocytophilum and the Lyme disease spirochete Borrelia burgdorferi induced glycolysis during infection and inhibition of oxidative phosphorylation enhanced microbial colonization of tick cells. Through an unbiased metabolomics approach, we discovered that β-aminoisobutyric acid (BAIBA) was an important metabolite for tick-microbe interactions. Whereas distinct levels of BAIBA affected tick weight and survival in vivo, disrupting BAIBA levels through genetic manipulation of catabolic enzymes reduced bacterial infection and restores tick fitness. Collectively, the metabolite BAIBA draws antagonistic pleiotropy on seemingly unrelated evolutionary traits in Ixodes scapularis ticks. Bioenergetics and resource allocation have yet to be explored as a strategy to constrain the public health burden of arthropod-borne diseases.