This study aimed to investigate the genomic and epidemiological features of a methicillin-resistant Staphylococcus aureus sequence type 1 (MRSA ST1) strain associated with caprine subclinical mastitis. An S. aureus strain was isolated from goat's milk with subclinical mastitis in Paraiba, Northeastern Brazil, by means of aseptic procedures and tested for antimicrobial susceptibility using the disk-diffusion method. Whole genome sequencing was performed using the Illumina MiSeq platform. After genome assembly and annotation, in silico analyses, including multilocus sequence typing (MLST), antimicrobial resistance and stress-response genes, virulence factors, and plasmids detection were performed. A comparative SNP-based phylogenetic analysis was performed using publicly available MRSA genomes. The strain showed phenotypic resistance to cefoxitin, penicillin, and tetracycline and was identified as sequence type 1 (ST1) and spa type 128 (t128). It harbored the SCCmec type IVa (2B), as well as the lukF-PV and lukS-PV genes. The strain was phylogenetically related to six community-acquired MRSA isolates (CA-MRSA) strains associated with human clinical disease in North America, Europe, and Australia. This is the first report of a CA-MRSA strain associated with milk in the Americas. The structural and epidemiologic features reported in the MRSA ST1 carrying a mecA-SCCmec type IVa suggest highly complex mechanisms of horizontal gene transfer in MRSA. The SNP-based phylogenetic analysis suggests a zooanthroponotic transmission, i.e., a strain of human origin.