Plastic pollution is widely recognised as a threat to life in our oceans and current trends indicate that the marine plastic burden and its ecological impact will continue to escalate. However, investigations of plastic pollution on marine microbial communities largely focus on microbes that attach to plastics, whereas impacts of plastic debris-leached chemicals remain poorly understood. We set out to investigate the impact of plastic leachate on natural communities of marine microbes using microcosm experiments, monitoring impacts on both the structure and function of this community. Our results show that exposure to leachate from polyvinyl chloride (PVC) matting negatively impact a broad group of photosynthetic microbes, both bacterial and eukaryotic, causing sharp declines in cell abundance, photosynthetic efficiency, and total chlorophyll. Further, PVC leachate impacted both taxonomic and functional diversity of the entire microbial community, with dramatic decreases in the abundance of key marine taxa including Synechococcus, SAR11 and members of the Rhodobacterales. Functional gene and metagenome-derived genome analyses showed that, while some key groups decline, fast-adapting, motile organisms were enriched, as were genes usually associated with pathogenicity and an increased capacity to metabolise organic compounds leached from PVC. These results reveal that PVC leachates have the potential to impact key organisms at the base of the marine food web, which could have significant flow-on effects for entire marine ecosystems. We are now investigating how specific components of the plastic leachate contribute to its toxicity to photosynthetic marine microbes.