Healthcare in low- and middle-income countries is becoming problematic due to the emergence of multidrug-resistant bacteria causing serious morbidity and mortality. carrying multiple antimicrobial resistance (AMR) genes were found significantly among sepsis patients in a study done between October 2019 and September 2020 at four Ethiopian hospitals located in the central (Tikur Anbessa and Yekatit 12), southern (Hawassa), and northern (Dessie) parts. Among 1416 sepsis patients, 74  isolates were identified using MALDI-TOF, most of them at Dessie ( = 44) and Hawassa ( = 28) hospitals. Whole genome sequencing showed that strains identified at Dessie Hospital displayed phylogenetic clonality, carried an IncM1 plasmid and the majority were ST3924. Many identified at Hawassa Hospital were clonally clustered and the majority belonged to novel STs and carried IncFIB(K) and IncFII(K) plasmids concurrently. Fifty carried ESBL genes while 2 isolates harboured AmpC. Other frequently found genes were , , , , , , , and . Virulence genes detected at both sites were for biofilm formation and siderophore ABC transporter operons for iron uptake. Capsular alleles varied, with at Dessie and at Hawassa. The isolation of multidrug-resistant as an emerging sepsis pathogen calls for strong infection prevention strategies and antimicrobial stewardship supported by advanced bacterial identification techniques.