The current lack of knowledge on the trophic ecology of scyphozoans, particularly at the benthic stage, prevents a full understanding of the controls on many jellyfish blooms. The blooming scyphozoan (Aurelia coerulea) completes its entire life cycle in the Thau lagoon (southern France), where the annual population dynamics of both its benthic and pelagic stages have been described. This offered an exceptional framework to investigate the trophic processes regulating jellyfish populations over time. To this aim, stable isotopic signature analysis (δ13C and δ15N) was used to infer the diet of both A. coerulea scyphistomae and medusae over 1 year. These results were matched with medusae gut content analysis and with the monthly abundances of local plankton groups. Lastly, the isotopic signatures of A. coerulea scyphistomae and medusae were compared with those of the oysters (Crassostrea gigas) cultivated in the lagoon to evaluate the potential interspecific trophic competition. The results revealed two seasonal shifts in the trophic niche of A. coerulea and substantial overlap between the diets of its benthic and pelagic stages. Conversely, trophic niche overlaps with the oysters were restricted, suggesting a limited impact of the local jellyfish bloom on shellfish production. Phytoplankton, microzooplankton, mesozooplankton, and sedimentary organic matter were all important food sources during critical periods of A. coerulea life-cycle. However, microzooplankton abundance was found to be key for the production of buds by the scyphistomae and, therefore it is likely to control the benthic population size and, thereby, to modulate the intensity of its annual bloom in Thau.