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Background: The potato tuber moth (PTM), Phthorimaea operculella (Zeller) (Lepidoptera: Gelechiidae), is a destructive pest of Solanaceae crops worldwide. α-solanine and α-chaconine are toxic steroidal glycoalkaloids (SGAs) in Solanaceae crops and are most abundant in potatoes (Solanum tuberosum L.), accounting for more than 95% of the total SGAs. PTM grows on potatoes with a higher concentration of SGAs. Gut bacteria play an important role in the physiology and behavior of insects. To understand the role of gut bacteria of PTM in host adaptability, we isolated and identified major SGA (α-chaconine and α-solanine)-degrading gut bacteria in the gut of PTM by a selective medium and analyzed their degradability and degradation mechanism., Results: The gut Glutamicibacter halophytocola S2 of PTM with high degradation capacity to α-solanine and α-chaconine were detected by liquid chromatography mass spectrometry (LC-MS) and identified by morphological and 16S rRNA gene sequence analysis. A gene cluster involving α-rhamnosidases, β-glucosidases, and β-galactosidases was identified by whole-genome sequencing of G. halophytocola S2. These genes had higher expression on the α-solanine medium. PTM inoculated with the isolated G. halophytocola S2 obtained higher fitness than antibiotic-treated PTM., Conclusion: The G. halophytocola S2 in the gut of PTM could degrade the major toxic α-solanine and α-chaconine in potatoes. This enhances the fitness of PTM feeding on potatoes with high SGA contents. The results provide a theoretical foundation for the integrated pest management of PTM and provide an effective strain for the treatment of α-solanine and α-chaconine in potato food. © 2022 Society of Chemical Industry., (© 2022 Society of Chemical Industry.)