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This study investigated the frequency of carbapenem and colistin resistance in ESBL-producing <i>K. pneumoniae</i> (ESBLK) isolates recovered from chickens and their environment, contact farm workers and hospitalized patients in Egypt. Further, the phenotypic and genotypic relationships between the community and hospital-acquired <i>K. pneumoniae</i> isolates in the same geographical area were investigated. From 272 total samples, 37 (13.6%) <i>K. pneumoniae</i> isolates were identified, of which 20 (54.1%) were hypervirulent. All isolates (100%) were multidrug-resistant (MDR) with multiple antibiotic resistance (MAR) indices ranging from 0.19 to 0.94. Colistin-resistant isolates (18.9%) displayed colistin MIC values >2 μg/mL, all harbored the <i>mcr</i>-1 gene. All isolates from patients (13/90, 14.4%), workers (5/22, 22.7%), chickens (9/100, 9%) and the environment (10/60, 16.7%) harbored a single or multiple β-lactamase genes, <i>bla</i>_SHV, <i>bla</i>_TEM, <i>bla</i>_CTX-M1 and <i>bla</i>_OXA-1, often in combination with carbapenemase genes (<i>bla</i>_VIM, <i>bla</i>_NDM-1 or <i>bla</i>_IMP; 45.9%), the <i>mcr</i>-1 gene (18.9%) or both (13.5%). Enterobacterial repetitive intergenic consensus (ERIC)–PCR genotyping revealed 24 distinct ERIC types (ETs) with a discrimination index of 0.961. Six ETs showed clusters of identical isolates from chicken and human sources. The increased frequency and genetic relatedness of ESBLK and carbapenemase-producing <i>K. pneumoniae</i> (CPK) from chickens and humans pose a public health threat that urge more prudent use of antimicrobials in chicken farms to avoid the propagation and expansion of both ESBLK and CPK from the chicken sources to humans.