Elizabethkingia genus is an aerobic, non-motile, non-spore forming Gram-negative bacilli that reside taxonomically within the family Flavibacteriaceae of phylum Proteobacteria. They are commonly found in the environment, particularly in soil and freshwater bodies, as well as insects and amphibians. Interest in these organisms is rising as they represent a difficult to treat opportunistic pathogen. In recent years, advances in diagnostic tools have greatly improved our understanding of causative agents and have revealed Elizabethkingia anophelis and Elizabethkingia meningoseptica as common human opportunistic pathogens in hospitals and healthcare settings. Many members of Flavobacteriaceae encode chromosomal β-lactamases, and genes encoding carbapenemases and cephalosporinases are unique within the Elizabethkingia genus, including blaB, blaGOB and blaCME. Given the potential broad-spectrum drug resistance these species possess, identifying Elizabethkingia spp. reservoirs will potentially help track and reduce the risk of future infection. Here, we characterized whole-genome sequences of Elizabethkingia species carrying multiple wide-spectrum metallo-β-lactamase (blaB and blaGOB) and the extended-spectrum serine-β-lactamase (blaCME) genes from Australian aquatic environments and performed comparative phylogenomic analyses against national clinical and international strains. Antibiotic MIC (Minimum Inhibitory Concentration) testing was performed on representative strains and showed significant resistance to carbapenems and cephalosporins but general susceptibility to fluoroquinolones, tetracyclines and trimethoprim-sulfamethoxazole. qPCR was also performed to quantify the levels of Elizabethkingia species in the source environments. A novel clade (n=7) was identified in our study which carried novel alleles of both metallo-β-lactamase and extended-spectrum serine-β-lactamase genes. Phylogenetics show that three environmental Elizabethkingia anophelis isolates are closely related to Elizabethkingia anophelis from Australian clinical isolates (~36 SNPs), and certain genomic signatures provide insight into potentially shared origins and a capacity to transfer mobile genetic elements with both national and international isolates.