In the small dairy holding settings, human, animal, environment, and awareness contribute significantly to the virulence and spreading dynamics of S. aureus pathogens. This study aims to trace the virulence characteristics of S. aureus causing bovine subclinical mastitis and the likelihood of their transmission to dairy products through apparently normal milk. One hundred and 50 California Mastitis Test positive milk samples were aseptically obtained from cows and buffalos owned by small dairy holders, as well as 75 samples of Egyptian raw milk cheese were collected from retailers at the same confined geographical district of milk sampling, in Monofiya Governorate, Egypt. Isolates were subjected to detailed biochemical characterization using SP-18 ID test followed by amplification and partial sequencing of the 16S rRNA gene to confirm isolates identities. Twenty-five S. aureus strains have been defined eventually. All the strains were subject to antimicrobial susceptibility testing against 18 antimicrobial compounds using the broth microdilution method. Twenty-five S. aureus strains showed 13 resistance patterns, involving 12 patterns with multidrug resistance. The proportion of antibiotic resistant strains was higher for ampicillin (25/25, 100%) and oxacillin (15/25, 60%). Fourteen MRSA strains were confirmed by detecting mecA gene and Staphylococcus Cassette Chromosome mec (SCCmec) classification. As a result, 7, 5 and 1 strains were classified into classes V, IV, and VI respectively, and one strain harbored 2 CCR genes (class 5C2&1). All isolates were examined for 11 SE genes, pvl, tsst, and 15 antimicrobial resistance genes. Moreover, the phylogenetic analysis of nucleotide sequence of Staphylococcus protein A gene (spa typing) revealed similarities between some MRSA and MSSA strains. This study identified a novel spa type “t18546” of a MSSA strain, and another MRSA strain, SCCmec IV/pvl⁺, showing the universal characteristics of the community associated (CA)-MRSA. Transformation of human and animal-associated S. aureus may occur in animals udder, rendering their transmission highly incident and hazardous.