Plastic pollution pervades aquatic ecosystems worldwide, releasing leachates that interact intimately with microbial communities. Antibiotic resistance genes (ARGs) disseminate rapidly through horizontal gene transfer via plasmid conjugation, posing a severe and accelerating threat to public health and environmental stability. While microplastic particles are known to promote ARG exchange within biofilms, the influence of soluble chemical leachates derived from degrading plastics has remained unclear. Here we show that photodegraded leachate from polyvinyl chloride (PVC)—a widely used material in water infrastructure—substantially enhances conjugative transfer of ARGs in both laboratory model systems and natural aquatic microbiomes. Exposure increased transconjugant abundance up to 26.4-fold and conjugation efficiency up to 44.6-fold, with non-monotonic responses modulated by leachate concentration and microbial community diversity. Characterization of the leachate revealed high proportions of biolabile dissolved organic matter alongside additives; mechanistic assays demonstrated that these effects arise through elevated intracellular reactive oxygen species (21% increase), activation of the SOS response and DNA-repair pathways, increased extracellular protein production facilitating cell–cell contact, and compensatory adjustments in the electron transport chain that maintain ATP homeostasis. These results demonstrate that plastic leachates act as potent but previously overlooked facilitators of ARG dissemination beyond the physical effects of microplastics. Our findings reveal a critical synergy between plastic pollution and the global antimicrobial-resistance crisis, underscoring the urgent need for targeted regulations on plastic additives and degradation products in aquatic systems.