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<i>Staphylococcus pseudintermedius</i> is frequently associated with several bacterial infections in dogs, highlighting a One Health concern due to the zoonotic potential. Given the clinical significance of this pathogen, we performed comprehensive genomic analyses of 28 <i>S. pseudintermedius</i> strains isolated from canine infections throughout whole-genome sequencing using Illumina HiSeq, and compared the genetic features between <i>S. pseudintermedius</i> methicillin-resistant (MRSP) and methicillin-susceptible (MSSP) strains. Our analyses determined that MRSP genomes are larger than MSSP strains, with significant changes in antimicrobial resistance genes and virulent markers, suggesting differences in the pathogenicity of MRSP and MSSP strains. In addition, the pangenome analysis of <i>S. pseudintermedius</i> from canine and human origins identified core and accessory genomes with 1847 and 3037 genes, respectively, which indicates that most of the <i>S. pseudintermedius</i> genome is highly variable. Furthermore, phylogenomic analysis clearly separated MRSP from MSSP strains, despite their infection sites, showing phylogenetic differences according to methicillin susceptibility. Altogether our findings underscore the importance of studying the evolutionary dynamics of <i>S. pseudintermedius</i>, which is crucial for the development of effective prevention and control strategies of resistant <i>S. pseudintermedius</i> infections.