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Background: <i>L. monocytogenes</i> and <i>L. ivanovii</i>, the only two pathogens of <i>Listeria</i>, can survive in various environments, having different pathogenic characteristics. However, the genetic basis of their excellent adaptability and differences in pathogenicity has still not been completely elucidated. Methods: We performed a comparative genomic analysis based on 275 <i>L. monocytogenes</i>, 10 <i>L. ivanovii,</i> and 22 non-pathogenic <i>Listeria</i> strains. Results: Core/pan-genome analysis revealed that 975 gene families were conserved in all the studied strains. Additionally, 204, 242, and 756 gene families existed uniquely in <i>L. monocytogenes</i>, <i>L. ivanovii,</i> and both, respectively. Functional annotation partially verified that these unique gene families were closely related to their adaptability and pathogenicity. Moreover, the protein–protein interaction (PPI) network analysis of these unique gene sets showed that plenty of carbohydrate transport systems and energy metabolism enzymes were clustered in the networks. Interestingly, ethanolamine-metabolic-process-related proteins were significantly enriched in the PPI network of the unique genes of the <i>Listeria</i> pathogens, which can be understood as a determining factor of their pathogenicity. Conclusions: The utilization capacity of multiple carbon sources of <i>Listeria</i> pathogens, especially ethanolamine, is the key genetic basis for their ability to adapt to various environments and pathogenic lifestyles.