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Jails have been hypothesized to be hotspots for the spread of methicillin-resistant Staphylococcus aureus (MRSA). We integrate genomic and epidemiologic data to investigate USA300 MRSA transmission in an urban jail and its connected communities. A genome-wide association study of 308 jail isolates from 2015-2018 revealed a plasmid encoding the ermC clindamycin/erythromycin resistance gene was associated with a 6-fold increased odds of MRSA genetic linkages among detainees. Additionally, 52% of jail-onset MRSA infections carried this plasmid compared to 14% of intake colonization isolates, supporting its role in MRSA spread in the jail. Extending our analysis to 774 isolates from a local healthcare system from 2011-2014, the ermC- carrying plasmid was also associated with MRSA transmission in the larger community and was enriched among former jail detainees and those with related isolates to recently incarcerated cases. Lastly, topical clindamycin exposure before MRSA infection was associated with ermC plasmid presence in both settings, but exposure prevalence was higher in jail versus community cases (7.5% vs. 0.9%), suggesting antibiotic use in the jail may have created a favorable environment for the spread of ermC -carrying strains. These findings highlight the impact of antibiotic use in jails on antibiotic resistance in both jails and their surrounding communities.