The Elizabethkingia genus has gained global attention in recent years as a nosocomial pathogen. Elizabethkingia spp. are intrinsically multidrug resistant, primarily infect immunocompromised individuals, and are associated with high mortality (~20-40%). Although Elizabethkingia infections appear sporadically worldwide, gaps remain in our understanding of transmission, global strain relatedness and patterns of antimicrobial resistance. To address these knowledge gaps, 22 clinical isolates collected in Queensland, Australia, over a 16-year period along with six hospital environmental isolates were examined using MALDI-TOF MS (VITEK MS) and whole-genome sequencing to compare with a global strain dataset. Phylogenomic reconstruction against all publicly available genomes (n=100) robustly identified 22 E. anophelis, three E. miricola, two E. meningoseptica and one E. bruuniana from our isolates, most with previously undescribed diversity. Global relationships show Australian E. anophelis isolates are genetically related to those from the USA, England and Asia, suggesting shared ancestry. Genomic examination of clinical and environmental strains identified evidence of nosocomial transmission in patients admitted several months apart, indicating probable infection from a hospital reservoir. Furthermore, broth microdilution of the 22 clinical Elizabethkingia spp. isolates against 39 antimicrobials revealed almost ubiquitous resistance to aminoglycosides, carbapenems, cephalosporins and penicillins, but susceptibility to minocycline, levofloxacin and trimethoprim/sulfamethoxazole. Our study demonstrates important new insights into the genetic diversity, environmental persistence and transmission of Australian Elizabethkingia species. Furthermore, we show that Australian isolates are highly likely to be susceptible to minocycline, levofloxacin and trimethoprim/sulfamethoxazole, suggesting that these antimicrobials may provide effective therapy for Elizabethkingia infections.