The etiologic agent of Chagas disease, Trypanosoma cruzi, is transmitted by hematophagous insect vectors that subsist on repeated blood meals over their lives separated by periods of fasting. Using naturally infected Mepraia spinolai, we measured the influence of parasite infection on this host vector's mortality during regular feeding and after fasting. After their capture, the insects were fed twice with uninfected mice to evaluate parasitic infection in their fecal samples by microscopic observation and PCR. Then the insects were subjected to a fasting period, followed by a third (final) feeding. After each feeding, a fecal sample was obtained to evaluate T. cruzi infection. To determine its progress through ontogeny, mortality and ecdysis of the infected and uninfected nymphs and adults were recorded on three occasions, over 140 d, and analyzed. Detections of infection by T. cruzi between the two first feedings increased, but this detection level was generally reduced after final feeding unless reinfected. For nymphs (stages III-V), their mortality was highest when infected after the fasting period, whereas adults were equally resistant to death after fasting when infected with T. cruzi. Metacyclic trypomastigotes were principally excreted in the fecal samples. Our results confirm that T. cruzi is pathogenic to its invertebrate hosts under nutritional stress conditions, when nymphs' mortality is higher while infected than uninfected when they were hungry. These results are epidemiologically important because T. cruzi harms the fasting vector M. spinolai, reducing its lifespan and competence as a disease vector, and thereby its rates of parasite transmission.