Currently, the spread of antimicrobial resistance (AMR) is a global trend and poses a severe threat to public health. The causative agent of cholera, a severe infectious disease with pandemic expansion, becomes more and more resistant to a wider range of drugs with every coming year. The Vibrio cholerae genome is highly flexible and adaptive; the acquisition of the SXT mobile element with a cluster of antibiotic resistance genes on it has marked a new stage in the adaptive evolution of the pathogen. The territory of Siberia and the Russian Far East is free of cholera; however, in the 1970s and 1990s a number of infection importation cases and acute outbreaks associated with the cholera importation were reported. The aim of this study was to describe the phenotypic characteristics and genetic determinants of AMR in V. cholerae strains isolated during epidemic complications in Siberia and the Far East of Russia, as well as to clarify the origin of the strains. The present research comprises analysis of nine V. cholerae El Tor strains isolated from patients and water sources during epidemic complications in Siberia and the Russian Far East in the 1990s. Here, we compared the phenotypic manifestations of antibiotic resistance among strains, harbored the resistance patterns in genomes; we also determined the structure, the type of SXT elements, and the mobilome profile based on the accepted classification. We identified that strains that caused outbreaks in Vladivostok and Yuzhno-Sakhalinsk in 1999 had ICEVchCHN4210 type SXT element with deletion of some loci. The research shows that the integration of the genome, SNP and the mobilome, associated with antibiotic resistance, analyses is necessary to understand the cholera epidemiology, it also helps to establish the origin of strains. The study of resistance determinants features allowed to make a conclusion about the heterogeneity of V. cholerae strains that were isolated during outbreaks in Vladivostok and Yuzhno-Sakhalinsk in 1999.