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Abstract The outcome of species competition strongly depends on the traits of the competitors and associated trade‐offs, as well as on environmental variability. Here, we investigate the relevance of consumer trait variation for species coexistence in a ciliate consumer–microalgal prey system under fluctuating regimes of resource supply. We focus on consumer competition and feeding traits, and specifically on the consumer's ability to overcome periods of resource limitation by mixotrophy, that is, the ability of photosynthetic carbon fixation via algal symbionts in addition to phagotrophy. In a 48‐day chemostat experiment, we investigated competitive interactions of different heterotrophic and mixotrophic ciliates of the genera Euplotes and Coleps under different resource regimes, providing prey either continuously or in pulses under constant or fluctuating light, entailing periods of resource depletion in fluctuating environments, but overall providing the same amount of prey and light. Although ultimate competition results remained unaffected, population dynamics of mixotrophic and heterotrophic ciliates were significantly altered by resource supply mode. However, the effects differed among species combinations and changed over time. Whether mixotrophs or heterotrophs dominated in competition strongly depended on the genera of the competing species and thus, species‐specific differences in the minimum resource requirements that are associated with feeding on shared prey, nutrient uptake, light harvesting, and access to additional resources such as bacteria. Potential differences in the curvature of the species' resource‐dependent growth functions may have further mediated the species‐specific responses to the different resource supply modes. Overall, our study demonstrates that genus‐ or species‐specific traits other than that related to nutritional mode may override the relevance of acquired phototrophy by heterotrophs in competitive interactions, and that the potential advantage of photosynthetic carbon fixation of symbiont‐bearing mixotrophs in competition with pure heterotrophs may differ greatly among different mixotrophs, playing out under different environmental conditions and depending on the specific requirements of the species. Complex trophic interactions determine the outcome of competition, which can only be understood by taking on a multidimensional trait perspective.