The stability of nutrient exchange in a mutualistic symbiosis is highly dependent on the availability of resources to both partners, and interactions between partners can shape niche partitioning among holobionts. Symbiotic sea anemones on California rocky shores obtain nitrogen and carbon from prey that they capture, but a large portion of their dietary carbon comes from contributions by symbiotic dinoflagellate algae in the family Symbiodiniaceae. We hypothesize that life history traits including allometry, surface-area-to-volume ratios, and reproductive strategies affect the potential for contributions from the algal symbionts. Our approach includes both observational and experimental studies of three congeneric sea anemone species. Anthopleura xanthogrammica is the largest species, A. sola is smaller, and A. elegantissima is the smallest, reproducing asexually to create large clonal mats. We designed an in situ experiment where the diets of sea anemones were manipulated by either adding or removing prey daily for three weeks. Tissue samples of sea anemone, algal symbiont, and common prey items were collected from the experiment and from an adjacent site for carbon and nitrogen stable isotope analysis. The δ15N values suggest that the diets of sea anemone species are different even though the anemones are found in the same habitat. The δ13C values are similar between A. sola and A. xanthogrammica but both are different from A. elegantissima values. We found that δ13C values of A. elegantissima anemone tissue and associated algal symbionts closely match while A. sola and A. xanthogrammica anemone tissue and algal symbiont δ13C do not match. This suggests that A. elegantissima relies mostly on algal symbiont contributions for its dietary carbon intake while A. sola and A. xanthogrammica receive a larger portion of their dietary carbon from heterotrophic feeding.