Parasites frequently share their host populations with other parasites. However, little is known about how different parasites respond to competition with diverse competitor species in the within-host and between-host environments. We explored the repeatability of competition by simultaneously exposing microcosm populations of the ciliate Paramecium caudatum to pairs of parasites from the Holospora species complex (H. undulata, H. caryophila and H. obtusa) affected the persistence and prevalence of each compared to single infections, across three host genotypes. Three weeks post-inoculation we identified the presence of each parasite using fluorescence in situ hybridisation (FISH). Competitive exclusion (62/72) was more common than co-existence (10/72) in populations inoculated with 2 parasites. There was a clear pattern of competitive superiority, with H. caryophila persisting in all doubly inoculated populations (with either H. undulata or H. obtusa), and H. undulata tending to exclude H. obtusa. This mirrored infection success in single infections, with H. caryophila having a higher infection prevalence in single inoculations, followed by H. undulata then H. obtusa. The probability of persistence in co-inoculations did not change across the different host genotypes, and prevalence was the same as in single infections. Our results are consistent with superinfection models, which assume the competitive exclusion of parasites upon contact within the same host. Furthermore, such non-random competitive epidemiological dynamics, where one parasites always wins, may be of interest for public health management, especially if the winning parasite is avirulent, as is seemingly the case here.