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This work aimed to characterize <i>S. aureus</i> isolates from the eyes of healthy and clinically affected equines in the Kafrelsheikh Governorate, Egypt. A total of 110 animals were examined for the presence of <i>S. aureus</i>, which was isolated from 33 animals with ophthalmic lesions and 77 healthy animals. We also investigated the antimicrobial resistance profile, oxacillin resistance mechanism, and the major virulence factors implicated in many studies of the ocular pathology of pathogenic <i>S. aureus</i>. The association between <i>S. aureus</i> eye infections and potential risk factors was also investigated. The frequency of <i>S. aureus</i> isolates from clinically affected equine eyes was significantly higher than in clinically healthy equids. A significant association was found between the frequency of <i>S. aureus</i> isolation from clinically affected equine eyes and risk factors including age and season but not with sex or breed factors. Antimicrobial resistance to common antibiotics used to treat equine eyes was also tested. Overall, the isolates showed the highest sensitivity to sulfamethoxazole (100%) and the highest resistance to cephalosporin (90.67%) and oxacillin (90.48%). PCR was used to demonstrate that <i>mecA</i> was present in 100% of oxacillin- and β-lactam-resistant <i>S. aureus</i> strains. The virulence factor genes <i>Spa</i> (x region), <i>nuc</i>, and <i>hlg</i> were identified in 62.5%, 100%, and 56%, of isolates, respectively, from clinically affected equines eyes. The severity of the eye lesions increased in the presence of γ-toxin-positive <i>S. aureus</i>. The phylogenetic tree of the <i>Spa</i> (x region) gene indicated a relationship with human reference strains isolated from Egypt as well as isolates from equines in Iran and Japan. This study provides insight into the prevalence, potential risk factors, clinical pictures, zoonotic potential, antimicrobial resistance, and β-lactam resistance mechanism of <i>S. aureus</i> strains that cause eye infection in equines from Egypt.