Combined exposure to stressors, including pesticides and pathogens, is common in natural insect populations. Pesticide resistance readily evolves in these populations and often coopts the same stress, detoxification, and immune pathways involved in physiological responses against primary pathogen and pesticide exposure. As a result, resistance evolution can alter antagonism or facilitation among chemical pesticides and pathogens in directions that remain difficult to predict. To investigate the interactive effects of chemical pesticide resistance, exposure, and bacterial infection on insect phenotypes, we experimentally evolved resistance to two different classes of pesticides (organophosphates and pyrethroids) in the red flour beetle, Tribolium castaneum. We exposed pesticide susceptible and resistant lines to pesticides, the entomopathogen and biocontrol agent Bacillus thuringiensis (Bt), or both. Pesticide resistance and Bt exposure were individually associated with slower development, indicating sub-lethal fitness costs of resistance and infection, respectively. After organophosphate exposure, however, beetles developed more quickly and were more likely to survive if also exposed to Bt. We used RNAseq to examine the interactive effects of pesticide resistance, pesticide exposure, and Bt exposure on gene expression. Pyrethroid-resistant insects exhibited dampened immune responses to Bt infection relative to susceptible ones. In a similar vein, simultaneous exposure to organophosphates and Bt resulted in muted stress-associated transcriptional responses compared to exposure with only one factor. Our results suggest that direct and host-mediated indirect interactions among pathogens and pesticides may buffer the cost of exposure to host fitness-associated traits within generations but exacerbate trade-offs over evolutionary time.