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The global spread of plasmid-mediated mobile colistin resistance (<i>mcr</i>) genes threatens the vital role of colistin as a drug of last resort. We investigated whether the recurrent occurrence of specific <i>E. coli</i> pathotypes and plasmids in individual pig farms resulted from the continued presence or repeated reintroduction of distinct <i>E. coli</i> strains. <i>E. coli</i> isolates (<i>n</i> = 154) obtained from three pig farms with at least four consecutive years of <i>mcr</i> detection positive for virulence-associated genes (VAGs) predicting an intestinal pathogenic pathotype via polymerase chain reaction were analyzed. Detailed investigation of VAGs, antimicrobial resistance genes and plasmid Inc types was conducted using whole genome sequencing for 87 selected isolates. Sixty-one <i>E. coli</i> isolates harbored <i>mcr-1</i>, and one isolate carried <i>mcr-4</i>. On Farm 1, <i>mcr</i>-positive isolates were either edema disease <i>E. coli</i> (EDEC; 77.3%) or enterotoxigenic <i>E. coli</i> (ETEC; 22.7%). On Farm 2, all <i>mcr</i>-positive strains were ETEC, while <i>mcr</i>-positive isolates from Farm 3 showed a wider range of pathotypes. The <i>mcr-1.1</i> gene was located on IncHI2 (Farm 1), IncX4 (Farm 2) or IncX4 and IncI2 plasmids (Farm 3). These findings suggest that various pathogenic <i>E. coli</i> strains play an important role in maintaining plasmid-encoded colistin resistance genes in the pig environment over time.