Significance Planktonic microorganisms interact with each other in multifarious ways, ultimately catalyzing the flow of carbon and energy in diverse aquatic environments. However, crucial links associated with eukaryotic microparasites are still overlooked in planktonic networks. We addressed such links by studying cryptic interactions between parasitic fungi, phytoplankton, and bacteria using a model pathosystem. Our results demonstrate that parasitic fungi profoundly modified microbial interactions through several mechanisms (e.g., transferring photosynthetic carbon to infecting fungi, stimulating bacterial colonization on phytoplankton cells, and altering the community composition of bacteria and their acquisition of photosynthetic carbon). Hence, fungal microparasites can substantially shape the microbially mediated carbon flow at the base of aquatic food webs and should be considered as crucial members within plankton communities.