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<i>Bacillus thuringiensis</i> (<i>Bt</i>) represents one of the most economical biopesticides to date. It produces toxins with insecticidal activity against many agricultural pests, including members of the genus <i>Spodoptera</i>. However, <i>Bt</i> tolerance leads to inefficiency in biological control. To overcome this problem, discovering the hidden cause(s) for the evolution of insect tolerance against <i>Bt</i> is of great importance. We hypothesized that changes in the gut microbiota due to the frequent application of <i>Bt</i> is one of those hidden causes. To investigate this hypothesis, we studied the effect of <i>Bt</i> Cry1c application on the <i>Spodoptera littoralis</i> larval gut microbiota in both <i>Bt</i>-susceptible and <i>Bt</i>-tolerant populations. The results revealed changes in the diversity and abundance of gut bacterial composition between the susceptible and tolerant populations. A high abundance of <i>Enterococcaceae</i> was detected in the tolerant population. Interestingly, Cry1c tolerance eliminates the bacterial genera <i>Klebsiella</i> and <i>Serratia</i> from the larval midgut. These changes may confirm the mechanism developed by <i>Spodoptera</i> larvae to counteract <i>Bt</i> Cry1c toxicity. Understanding the <i>B. thuringiensis</i>–gut microbiota interaction may help in improving biocontrol strategies against agricultural pests to overcome the evolution of tolerance.