We measured how predator‐ and prey‐derived chemical cues affect swimming behaviors and encounter rates of two common phytoplankton species (Amphidinum carterae, Heterosigma akashiwo) and two heterotrophic dinoflagellate predators (Stoeckeria algicida, Gyrodiniellum shiwhaense). Using video and image analysis, the microscopic three‐dimensional movement behaviors and macroscopic population distributions of the species were quantified in response to chemical cues derived from their respective predator or prey species. S. algicida preferentially feeds on H. akashiwo but displayed significant increases in swimming speed and turning rate when exposed to filtrate from either prey species. Prey cue‐induced changes in predator swimming behavior resulted in an average 11% increase in encounter rate. S. algicida that respond to prey filtrate would reach their daily prey quota at a 25% lower ambient prey concentration. In contrast, G. shiwhaense, which rarely feeds and does not grow on H. akashiwo, exhibited no shifts in behavior in response to algal filtrate. Predator‐derived cues from S. algicida elicited significant increases in upward motility in H. akashiwo, resulting in a shift in the prey population abundance away from the predator‐derived chemical cue. These algal fleeing behaviors reduced estimated encounter rates by 4%, compared to non‐fleeing behaviors. Our results provide quantitative evidence for the importance of chemical cues in modulating feeding interactions and emphasize the ramifications of individual behaviors, and modulation thereof, to population‐level outcomes, including population distributions, and predation pressure.