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Enterococci are Gram-positive bacteria that can be isolated from a variety of environments including soil, water, plants, and the intestinal tract of humans and animals. Although they are considered commensals in humans, <i>Enterococcus</i> spp. are important opportunistic pathogens. Due to their presence and persistence in diverse environments, <i>Enterococcus</i> spp. are ideal for studying antimicrobial resistance (AMR) from the One Health perspective. We undertook a comparative genomic analysis of the virulome, resistome, mobilome, and the association between the resistome and mobilome of 246 <i>E. faecium</i> and 376 <i>E. faecalis</i> recovered from livestock (swine, beef cattle, poultry, dairy cattle), human clinical samples, municipal wastewater, and environmental sources. Comparative genomics of <i>E. faecium</i> and <i>E. faecalis</i> identified 31 and 34 different antimicrobial resistance genes (ARGs), with 62% and 68% of the isolates having plasmid-associated ARGs, respectively. Across the One Health continuum, tetracycline (<i>tetL</i> and <i>tetM</i>) and macrolide resistance (<i>ermB</i>) were commonly identified in <i>E. faecium</i> and <i>E. faecalis</i>. These ARGs were frequently associated with mobile genetic elements along with other ARGs conferring resistance against aminoglycosides [<i>ant(6)-la</i>, <i>aph(3′)-IIIa</i>], lincosamides [<i>lnuG</i>, <i>lsaE</i>], and streptogramins (<i>sat4</i>). Study of the core <i>E. faecium</i> genome identified two main clades, clade ‘A’ and ‘B’, with clade A isolates primarily originating from humans and municipal wastewater and carrying more virulence genes and ARGs related to category I antimicrobials. Overall, despite differences in antimicrobial usage across the continuum, tetracycline and macrolide resistance genes persisted in all sectors.