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Multidrug-resistant <i>Klebsiella pneumoniae</i> (MDR <i>Kp</i>), in particular carbapenem-resistant <i>Kp</i> (CR-<i>Kp</i>), has become endemic in Italy, where alarming data have been reported on the spread of colistin-resistant CR-<i>Kp</i> (CRCR-<i>Kp</i>). During the period 2013–2014, 27 CRCR-<i>Kp</i> nosocomial strains were isolated within the Modena University Hospital Policlinico (MUHP) multidrug resistance surveillance program. We retrospectively investigated these isolates by whole-genome sequencing (WGS) analysis of the resistome, virulome, plasmid content, and core single nucleotide polymorphisms (cSNPs) in order to gain insights into their molecular epidemiology. The in silico WGS analysis of the resistome revealed the presence of genes, such as <i>blaKPC</i>, related to the phenotypically detected resistances to carbapenems. Concerning colistin resistance, the plasmidic genes <i>mcr</i> <i>1–9</i> were not detected, while known and new genetic variations in <i>mgrB</i>, <i>phoQ</i>, and <i>pmrB</i> were found. The virulome profile revealed the presence of type-3 fimbriae, capsular polysaccharide, and iron acquisition system genes. The detected plasmid replicons were classified as <i>IncFIB(pQil)</i>, <i>IncFIB(K)</i>, <i>ColRNAI</i>, <i>IncX3</i>, and <i>IncFII(K)</i> types. The cSNPs genotyping was consistent with the multi locus sequence typing (MLST) and with the distribution of mutations related to colistin resistance genes. In a nosocomial drug resistance surveillance program, WGS proved to be a useful tool for elucidating the spread dynamics of CRCR-<i>Kp</i> nosocomial strains and could help to limit their diffusion.