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Urinary tract infections (UTIs), traditionally dominated by Gram-negative pathogens, are increasingly complicated by antimicrobial-resistant Enterococcus spp. in hospital settings, particularly during the use of indwelling catheters. This study screened urine samples from 210 catheterized intensive care unit patients at Uppsala University Hospital (June 2020–September 2021), identifying 39 unique PhenePlate™-RF types across E. faecium, E. faecalis, and E. durans. E. faecium isolates showed considerable diversity, primarily within clonal complex 17 (CC17), known for its virulence and antibiotic resistance. We identified multiple lineages and sequence types (STs), such as in patient HWP143, who had isolates from both ST80 and ST22 (an ancestral CC17 lineage). Notably, metabolic adaptations, such as increased L-arabinose metabolism, and shifts in antibiotic resistance were observed. Variations and similarities in plasmid content between individual lineages suggest horizontal gene transfer. E. faecalis isolates exhibited less diversity, but still significant metabolic variability across patients and mixed infections, as seen in patient HWP051, colonized by both ST16 (CC58) and ST287. E. durans, though less common, shared important metabolic traits with E. faecium and displayed polyclonal characteristics, highlighting its potential role in UTIs and the complexity of enterococcal infections. E. durans was sometimes misidentified, underlining the need for accurate identification methods. This research underscores the importance of understanding genetic and metabolic diversity, plasmid variations, and horizontal gene transfer (HGT) in Enterococcus spp., which influence antibiotic resistance, virulence, and ultimately, treatment outcomes.