Avian pathogenic Escherichia coli (APEC) are a leading cause of extraintestinal infections in poultry. While conjugative ColV plasmids are known to promote APEC virulence and persistence at extraintestinal sites, their impact on bacterial fitness within the gut, an important reservoir of both pathogenic and commensal E. coli, remains unclear. This study investigated how ColV plasmid carriage influences APEC maintenance and transmission within the avian microbiota, with implications for controlling plasmid-mediated virulence in poultry production. Using a bespoke in vitro avian gut model, we examined the effect of the ColV plasmid pCB001 on the maintenance and proliferation of APEC and commensal E. coli. Two isogenic isolate pairs were compared: an ST-117 APEC parent carrying ColV and its plasmid-cured derivative, and an ST-373 commensal isolate and its ColV transconjugant. Each was introduced independently and in co-culture within caecal microbial communities. Growth kinetics and microbial community composition were assessed using culture-based enumeration and metataxonomic sequencing. ColV plasmid carriage enhanced persistence in both lineages, but competitive outcomes depended on host background and co-culture context. In independent culture, the APEC parent attained the highest densities. In co-culture, the commensal outcompeted the plasmid-cured APEC regardless of its own plasmid status. When both lineages carried pCB001, the commensal again predominated, whereas the APEC isolate dominated only when it alone carried the plasmid. These findings highlight that ColV plasmids confer adaptive benefits extending beyond pathogenic niches, differentially influencing bacterial fitness across host backgrounds and shaping the persistence and population dynamics of commensal E. coli within the gut ecosystem.