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Cephalosporins and polymyxins are employed in antimicrobial protocols to control and treat neonatal infections and post-weaning diarrhoea in swine operations. We conducted a longitudinal study to evaluate the colonization and transmission of antibiotic–resistant <i>Escherichia coli</i> in sows and their piglets in a farrow-to-finish operation, focusing on characterization of Extended Spectrum Beta-Lactamase (ESBL) and <i>mcr</i> genes, virulence traits and genetic relatedness. A total of 293 <i>E. coli</i> isolates were obtained from faecal samples collected in five time points. At birth <i>bla</i>_CTX-M-1group cluster was detected in <i>E. coli</i> isolates from 9 sows and 49 piglets (73.41%), while in the following four’ piglets sampling moments it was detected in 91.8%, 57.6%, 71.4% and 97.4%. The gene <i>mcr</i>-<i>1</i> was detected in <i>E. coli</i> from one sow and from three piglets from different litters at birth and increased in the first weeks of piglet life (68.85%, 100%, 90% and 8.1%). A new <i>mcr</i>-<i>4</i> allele, <i>mcr</i>-<i>4.7</i>, was identified in 3.28%, 28.57%, 7.5% of <i>E. coli</i> isolates. Most <i>mcr</i>-positive <i>E. coli</i> isolates (96,7%) carried <i>bla</i>_CTX-M-1Group genes and 93,33% carried both <i>mcr</i>-<i>4</i> and <i>mcr</i>-<i>1</i>. CTX-M-1 and CTX-M-32 were the most predominant ESBLs. Plasmids belonged to IncI1, IncF and IncN groups. Most isolates belong to phylogenetic group B1; PAI IV₅₃₆ marker was detected in nine isolates. The strains were kept in the different stages of the piglets’ life. The use of ceftiofur and colistin may explain the high prevalence and co-selection of <i>bla</i>_CTX-M-1Group and <i>mcr</i>-<i>1</i> and/or -<i>4</i> genes, contributing to the maintenance of resistant and virulent isolates throughout the pig life cycle that may reach the food chain.