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<i>Yersinia enterocolitica</i> culture-positive rodents and shrews were reported in different territories across Georgia during 14 of 17 years of investigations conducted for the period of 1981–1997. In total, <i>Y. enterocolitica</i> was isolated from 2052 rodents (15 species) and 33 shrews. Most isolates were obtained from <i>Microtus arvalis</i>, <i>Rattus norvegicus</i>, <i>Mus musculus</i>, and <i>Apodemus</i> spp. During the prospective study (2017−2019), isolates of <i>Yersinia</i>-like bacteria were cultured from 53 rodents collected in four parts of Georgia. All the <i>Yersinia</i>-like isolates were confirmed as <i>Y. enterocolitica</i> based on the API 20E and the BD Phenix50 tests. Whole-genome (WG) sequencing of five rodents and one shrew strain of <i>Y. enterocolitica</i> revealed that they possessed a set of virulence genes characteristic of the potentially pathogenic strains of biogroup 1A. All isolates lacked distinguished virulence determinants for YstA, Ail, TccC, VirF, and virulence plasmid pYV but carried the genes for YstB, YmoA, HemPR-HmuVSTU, YaxAB, PhlA, PldA, ArsCBR, and a flagellar apparatus. One strain contained a gene highly homologous to heat-labile enterotoxin, a chain of <i>E. coli</i>, a function not previously described for <i>Y. enterocolitica</i>. The WG single-nucleotide polymorphism-based typing placed the isolates in four distinct phylogenetic clusters.