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<i>Salmonella</i> Enteritidis was the primary foodborne pathogen responsible for acute gastroenteritis. The growing ceftriaxone resistance poses a significant threat to public health. Infection with <i>S.</i> Enteritidis has emerged as a major public health concern, particularly in developing countries. However, research on ceftriaxone-resistant <i>S.</i> Enteritidis (CRO-RSE) remains limited, particularly concerning its resistance mechanism, plasmid structure, and transmission characteristics. This study aims to address these gaps comprehensively. We collected 235 <i>S.</i> Enteritidis isolates from Hangzhou First People’s Hospital between 2010 and 2020. Among these, 8.51% (20/235) exhibited resistance to ceftriaxone. Whole-genome analysis revealed that 20 CRO-RSE isolates harbored <i>bla</i>_CTX-M-55 or <i>bla</i>_CTX-M-14 on the plasmid. Moreover, the dissemination of the <i>bla</i>_CTX-M-type gene was associated with IS<i>26</i> and IS<i>Ecp1</i>. Plasmid fusion entailing the integration of the p1 plasmid with antibiotic resistance genes and the p2 (pSEV) virulence plasmid was observed in certain CRO-RSE. Additionally, the structural analysis of the plasmids unveiled two types carrying the <i>bla</i>_CTX-M-type gene: type A with multiple replicons and type B with IncI1 (Alpha) replicon. Type B plasmids exhibited superior adaptability and stability compared to type A plasmids within <i>Enterobacteriaceae</i>. Interestingly, although the type B (S808-p1) plasmid displayed the potential to spread to <i>Acinetobacter baumannii</i>, it failed to maintain stability in this species.