Methicillin-resistant Staphylococcus aureus (MRSA) is a dynamic and tenacious pathogenic bacterium which is prevalent in livestock farming environments. This study investigated the possibility of MRSA spread via bioaerosol transmission from an indoor chicken farm environment to outdoors downwind (up to 50 m). The concentration of total airborne bacteria colony formation units (CFUs) was decreased with increasing sampling distance ranging from 9.18 × 101 to 3.67 × 103 per air volume (m3). Among the 21 MRSA isolates, 15 were isolated from indoor chicken sheds and exposure square areas, whereas 6 were isolated from downwind bioaerosol samples. Molecular characterization revealed that all of them carried the staphylococcal cassette chromosome mec (SCCmec) VIII, and they were remarkably linked with the hospital-associated MRSA group. Spa typing analysis determined that all MRSA isolates belonged to spa type t002. Virulence analysis showed that 100% of total isolates possessed exfoliative toxin A (eta), whereas 38.09% and 23.80% strains carried exfoliative toxin B (etb) and enterotoxin A (entA). Additionally, all of these MRSA isolates carried multidrug resistance properties and showed their resistance against chloramphenicol, ciprofloxacin, clindamycin, tetracycline, and erythromycin. In addition, chi-squared statistical analysis displayed a significant distributional relationship of gene phenotypes between MRSA isolates from chicken farm indoor and downwind bioaerosol samples. The results of this study revealed that chicken farm indoor air might act as a hotspot of MRSA local community-level outbreak, wherein the short-distance dispersal of MRSA could be supported by bioaerosols.