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We analyzed and compared genomes of Extended Spectrum Beta-Lactamase (ESBL)-producing <i>Escherichia coli</i> from pigs and pig farm workers at 116 farms in Vietnam. Analyses revealed the presence of <i>bla</i>_CTX-M-55, <i>bla</i>_CTX-M-27, <i>bla</i>_CTX-M-15, <i>bla</i>_CTX-M-14, <i>bla</i>_CTX-M-3, <i>bla</i>_CTX-M-65, <i>bla_CTX-M-24</i>, <i>bla_DHA-1</i>, and <i>bla_CMY2</i> in both hosts. Most strains from pigs contained quinolones (<i>qnr</i>) and colistin resistance genes (<i>mcr</i>-1 and <i>mcr</i>-3). Isolates predominantly harbored more than one plasmid replicon and some harbored plasmid replicons on the same contigs as the ESBL genes. Five strains from farm workers of ST38 (2), ST69 (1), and ST1722 (2) were classified as either uropathogenic <i>E. coli</i> (UPEC_HM)/extraintestinal pathogenic <i>E. coli</i> (ExPEC_JJ) or UPEC_HM, and the remaining were genetically distinct commensals. A high heterogeneity was found among the ESBL-producing <i>E. coli</i> from pigs and workers, with most isolates belonging to unrelated phylogroups, serogroups, and sequence types with >4046 Single-Nucleotide Polymorphisms-(SNPs). In comparing the genomes of pig isolates to those from humans, it appeared that ESBL-producing <i>E. coli</i> in workers did not predominantly originate from pigs but were rather host-specific. Nevertheless, the occurrence of ESBL-producing <i>E. coli</i> carrying plasmid-mediated colistin and quinolone resistance genes in pigs could represent a potential source for horizontal transmission to humans through food rather than direct contact.