Lactococcosis is a major bacterial disease impacting rainbow trout production in South Africa and Southeast Asia, particularly during the summer. This study analysed 15 bacterial isolates from affected aquaculture facilities, revealing that Lactococcus petauri (n=12) was the predominant species, rather than the traditionally recognised L. garvieae (n=3). This finding suggests a possible shift in the aetiology of lactococcosis, with potential implications for disease management. Genotypic analysis revealed that only L. garvieae isolates carried the adhesin gene (adh), which is critical for bacterial adhesion and colonisation. Most isolates possessed sortase-anchored proteins linked to iron uptake, adhesion, and stress resistance, with the LPxTG-6 subgroup unique to L. garvieae. Variations in the capsule operon, including transposase insertions, suggest ongoing horizontal gene transfer, possibly influencing immune evasion. Antimicrobial resistance (AMR) analysis identified efflux pumps ( mdtA, lsaD) conferring resistance to macrolides and lincosamides, with additional genotypic resistance to erythromycin ( mefA, msrD) and tetracyclines ( tetS, tetL). The presence of plasmid-borne tetL raises concerns about potential gene transfer and the persistence of resistance in aquaculture systems. Prophage elements were identified in several isolates, potentially contributing to virulence, and immune modulation. Although phage therapy has shown promise in experimental settings, the presence of viral defence mechanisms may raise a unique challenge. These findings highlight the importance of monitoring pathogen evolution in aquaculture systems and suggest that ongoing genomic surveillance and treatment strategies may need to be adapted to account for the emerging role of L. petauri in lactococcosis outbreaks.