Tribolium castaneum (Herbst) (Coleoptera:Tenebrionidae) has developed extensive resistance to the fumigant phosphine. Knowledge of the resistance mechanisms offers insight into resistance management. Although several studies have highlighted the positive or negative impacts of symbiotic microbiota on host pesticide resistance, little is known about the association between gut symbionts and host phosphine resistance. To reveal the effect of the gut bacterium, Enterococcus faecalis (Andrewes & Horder) (Lactobacillales: Enterococcaceae), on host phosphine resistance and its underlying mechanism, we investigated mortality, fitness, redox responses, and immune responses of adult T. castaneum when challenged with E. faecalis inoculation and/or phosphine exposure. When T. castaneum was exposed to phosphine, E. faecalis inoculation decreased its survival and female fecundity and aggravated its oxidative stress. Furthermore, E. faecalis inoculation suppressed the expression and activity of superoxide dismutase, catalase, and peroxidase in phosphine-exposed T. castaneum. Enterococcus faecalis inoculation also triggered excessive host immune responses, including the immune deficiency signaling pathway and the dual oxidase-reactive oxygen species system. These findings suggest that E. faecalis likely modulates host phosphine resistance by interfering with the redox system. This provides information for examining the symbiotic function in the insect-microorganism relationship and new avenues for pesticide resistance management.