The maintenance of two genetically distinct reproductive modes such as outcrossing and selfing within a population of animals or plants is still a matter of considerable debate. Hermaphroditic parasites often reproduce either alone by selfing or in pairs by outcrossing. They can be used as a model to study potential benefits of outcrossing. Any advantage from outcrossing may be important, especially in host-parasite coevolution, but has not, to our knowledge, been studied yet in any parasite species. We studied the potential effect of outcrossing in a tapeworm, Schistocephalus solidus, on both infection success and growth in its first intermediate host, the copepod Macrocyclops albidus. Tapeworms that had been obtained from natural populations of three-spined sticklebacks (Gasterosteus aculeatus) were allowed to reproduce either alone or in pairs, in an in vitro system that replaced the final host's gut. This resulted in either selfed or outcrossed offspring, respectively. In one part of the experiment, copepods were exposed to either selfed or outcrossed parasites, in a second part to both types simultaneously, in order to study the effect of competition between them. To discriminate parasites of either origin within the same host, a novel method for fluorescent vital labeling was used. We show here for the first time that outcrossed parasites had a higher infection success and faster development in the host. This advantage of outcrossing became apparent only in the competitive situation, in which superior abilities of parasites to extract limiting resources from the host become crucial.