While many studies have examined the impact of oil on phytoplankton or bacteria, very few considered the effects on the biological complex formed by phytoplankton and their associated phytoplankton-attached (PA) and free-living (FL) bacteria. However, associated bacteria can affect the physiology of phytoplankton and influence their stress responses. In this study, we monitored the growth of Heterocapsa sp., an armoured dinoflagellate, exposed to crude oil, Corexit dispersant, or both. Growth of Heterocapsa sp. is unaffected by crude oil up to 25ppm, a concentration similar to the lower range measured on Florida beaches after the Deepwater Horizon oil spill. The PA bacteria community was resistant to exposure, whereas the FL community shifted towards oil degraders; both responses could contribute to Heterocapsa sp. oil resistance. The growth rate of Heterocapsa sp. decreased significantly only when exposed to dispersed oil at 25ppm, indicating a synergistic effect of dispersant on oil toxicity in this organism. For the first time, we demonstrated the decoupling of the responses of the PA and FL bacteria communities after exposure to an environmental stress, in this case oil and dispersant. Our findings suggest new directions to explore in the understanding of interactions between unicellular eukaryotes and prokaryotes.