1. Aggregated distributions of parasite individuals across host individuals are nearly ubiquitous among parasitic taxa. The size and sex ratio of the population of one parasite species infecting a single host (hereafter “infrapopulation”) can influence parasite fitness through intraspecific competition, mate availability, and the ability to attract vectors for transmission of parasite propagules. Competition for both resources and for pollen and seed vector services may limit reproductive success (pollen receipt, fruit production, and seed dispersal) in large infrapopulations of parasitic plants, while mate limitation or reduced ability to attract vectors may limit this success in small infrapopulations. 2. Using a dioecious parasitic plant, desert mistletoe (Phoradendron californicum), we experimentally removed reproductive tissue from male parasites in whole infrapopulations to test for independent effects of infrapopulation size and within-host mate availability on female fitness. As desert mistletoe requires both pollen and seed vectors for successful reproduction, the species provides the opportunity to test how infrapopulation characteristics affect multiple components of parasite fitness. 3. We found that insect-mediated pollen receipt decreased for parasites on treated hosts, consistent with within-host mate limitation. Additionally, the relationship between mate availability and fruit production per flower ranged from neutral to positive depending on year of the experiment. 4. As expected if competition for host resources limits reproductive success more than mate availability in larger infrapopulations, the greater pollen receipt to females in large infrapopulations did not generally translate into increased mistletoe fruit production. Relationships between mistletoe fruit production per flower and infrapopulation size ranged from negative to neutral. 5. Both pollen receipt and pollinator visitation increased with infrapopulation size, indicating that larger populations can be more attractive to pollen vectors independent of mate availability. However, we found no relationship between infrapopulation size and fruit removal by dispersers and, thus, no evidence that attraction of seed dispersal vectors increases with infrapopulation size. 6. Synthesis: These results highlight the interactive roles of within-host processes (resource competition, mate availability, and vector attraction) in determining the fitness of biotically-transmitted parasite individuals.