Introduction Methicillin-resistant Staphylococcus aureus (MRSA) is a bacterial pathogen resistant to several widely used antibiotics. Although MRSA has historically been associated with hospital- and community-associated infections, livestock-associated MRSA (LA-MRSA) has emerged as a public health concern worldwide. While the majority of studies on LA-MRSA have focused on the CC398 lineage, little is known about the other lineages circulating in livestock. This study reports the whole-genome sequencing (WGS)-based characterization of 17 non-CC398 MRSA isolates with spa types typically associated with human infections. Methods The isolates were collected from healthy food-producing farm animals in Belgium between 2011 and 2021. WGS was used for typing and detecting antimicrobial resistance (AMR), virulence genes, and plasmids. Core genome multi-locus sequence typing (MLST) and single nucleotide polymorphism (SNP)-based phylogenomic analyses were performed to investigate the relationship between isolates and to compare them with publicly available genomic data. Results Five sequence types (STs) were identified: ST1 ( n = 1), ST22 ( n = 6), ST80 ( n = 1), ST239 ( n = 8), and ST612 ( n = 1), all belonging to clonal complexes other than the typical livestock-associated CC398. For ST22 and ST239, we identified several isolates that showed very high genomic similarity, indicating either transmission between farms or acquisition from a common source. For ST239, we identified a shared lineage among isolates collected from laying hens and cattle throughout the study period. A comparison with public datasets revealed a high genomic similarity between the isolates from this study and globally circulating human-associated lineages, suggesting shared ancestry and clonal spread rather than direct evidence of zoonotic transmission. Discussion This study provides insights into the genomic diversity, spread, and potential public health relevance of non-CC398 MRSA lineages circulating in Belgian livestock.