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A rising incidence of clinical infections has been caused by <i>Kluyvera</i>, a significant opportunistic pathogen. Meanwhile, <i>Kluyvera</i> acts as an important reservoir of <i>bla</i>_CTX-Ms, which are the dominant genes of class A extended-spectrum β-lactamases (ESBLs). In this work, 60 strains of <i>Kluyvera</i> were subjected to phylogenetic relationship reconstruction, antimicrobial susceptibility testing, and antibiotic resistance genes prediction. All mature <i>bla</i>_CTX-Ms were gathered to perform subgroup reclassification. The findings demonstrate that <i>Kluyvera</i> has a large gene pool with significant genetic flexibility. Notably, 25% of strains showed simultaneous detection of ESBLs and carbapenem resistance genes. The genotypes of fourteen novel <i>bla</i>_CTX-Ms were identified. A new subgroup classification approach for <i>bla</i>_CTX-Ms was defined by using 20 amino acid site variants, which could split <i>bla</i>_CTX-Ms into 10 subgroups. The results of the subgroup division were consistent with the phylogenetic clustering. More significantly, we proposed a novel <i>bla</i>_CTX-M subgroup, KLUS, that is chromosomally encoded in <i>K. sichuanensis</i> and the new species put forward in this study, showing amino acid differences from the currently known sequences. Cloning and transformation tests demonstrated that the recipient bacteria had a robust phenotype of cefotaxime resistance. Closely related <i>Kluyvera</i> species had <i>bla</i>_CTX-Ms in the same subgroup. Our research lays the groundwork for a deeper comprehension of <i>Kluyvera</i> and emphasizes how important a <i>bla</i>_CTX-M reservoir it is. We provide an update on <i>bla</i>_CTX-M subgroups reclassification from the aspects of phylogenetic relationship, amino acid differences, and the new subgroup KLUS, which needs to be strengthen monitored due to its strong resistance phenotype to cefotaxime.