The rate of polymyxin-resistant Enterobacteriaceae, as well as human and animal infections caused by them, is increasing worldwide, posing a high epidemiological threat since colistin represents a last-resort antibiotic to treat complicated infections. The study of environmental niches, in particular, aquatic ecosystems in terms of genome analysis of inhabiting antimicrobial-resistant (AMR) microorganisms as reservoirs of acquired resistance determinants (AMR genes), represents a specific concern from a One Health approach. Here, we present a phenotypic AMR analysis and molecular characterization of Escherichia coli isolate found in municipal drinking water after an accident in the water supply system of a residential building in Armenia in 2021. CrieF1144 E. coli isolate was resistant to ampicillin, ampicillin/sulbactam, cefuroxime, ciprofloxacin, levofloxacin, trimethoprim/sulfamethoxazole, colistin, and tigecycline, whereas whole genome sequencing (WGS) revealed blaTEM-1B, tet(A), and a combination of dfrA14 with sul1 resistance determinants, which corresponds well with phenotypic resistance above. Moreover, the multidrug-resistant isolate studied harbored mcr-1.1 gene on a conjugative 251 Kb IncHI2 plasmid, whose structure was determined using hybrid short- and long-reads assembly. CrieF1141_p1 plasmid carried all antimicrobial resistance genes revealed in the isolate and did not harbor any virulence determinants, so it could contribute to the spread of AMR genes in the bacterial population. Two copies of ISApl1 transposase-encoding element, which is likely to mediate mcr-1.1 gene mobilization, were revealed surrounding this gene in a plasmid.