In the past decade, gut microbiota has come to the fore in search for the cause of disregulation in intestinal homeostasis. Here, we report a possible link between gut microbial dynamics and stress-inducing factors using the leaf worm moth Spodoptera litura as a model organism. Investigation reveals that S. litura exhibits dysbiosis i.e. alteration in the gut microbiota composition that might induce or suppress inflammation upon exposure to dextran sulfate sodium salt, a tissue damaging agent (DSS, 40 kD). It primarily corresponds to an expansion of the bacterial phylotypes Enterobacter sp., Pseudomonas sp., Escherichia sp. and Acinetobacter sp. belonging to subclass Gammaproteobacteria. To assess the role played by gut residents in midgut inflammation, we re-colonized the axenic insects with Pseudomonas, Enterobacter and Acinetobacter individually. We observed that Pseudomonas and Enterobacter monoassociated insects exhibit inflammatory effects like damage to gut epithelium and hyperproliferation of stem cells under stress conditions. Conversely, Acinetobacter promotes fitness in larvae and reduces inflammatory effects of DSS. However, we failed to detect phenotypic inflammatory changes like midgut epithelium damage and stem cell proliferation in axenic insects reared on DSS-supplemented diet. Our results highlight that gut commensals that apparently remain low in abundance and benign under typical conditions can exert modulatory (positive or negative) effects on host fitness in the presence of stimulator.