Bacterial infections can substantially impact host metabolic health as a result of the direct and indirect demands of sustaining an immune response and of nutrient piracy by the pathogen itself. Drosophila melanogaster and other insects that survive a sublethal bacterial infection often carry substantial pathogen burdens for the remainder of life. In this study, we asked whether these chronic infections exact metabolic costs for the host, and how these costs scale with the severity of chronic infection. We infected D. melanogaster with four bacterial species (Providencia rettgeri, Serratia marcescens, Enterococcus faecalis and Lactococcus lactis) and assayed metabolic traits in chronically infected survivors. We found that D. melanogaster carrying chronic infections were uniformly more susceptible to starvation than uninfected controls, and that sensitivity to starvation escalated with higher chronic pathogen burden. We observed some evidence for greater depletion of triglyceride and glycogen stores in D. melanogaster carrying chronic bacterial loads, although this varied among bacterial species. Chronically infected flies exhibit sustained upregulation of the immune response, which we hypothesized might contribute to the metabolic costs. Consistent with this prediction, genetic activation of the major innate immune signaling pathways depleted metabolic stores and increased starvation sensitivity even in the absence of infection. These results demonstrate that even sublethal infections can have substantial health and fitness consequences for the hosts, arising in part from pathogen-induced immune activation, and that the consequences scale quantitatively with the severity of infection.