The success of parasitic life lies in an optimal exploitation of the host to satisfy key functions directly involved in reproductive fitness. Resource availability generally decreases over time with host mortality, but also during multiple infections, where different strains of parasite share host resources. During multiple infections, the number of parasite strains and their genetic relatedness are known to influence their reproductive rates. Using infections of the potato plant Solanum tuberosum with the parasite Phytophthora infestans, we set up an experimental design to separate dose effects (double- vs. single-site infections) from genetic relatedness (different vs. identical genotypes) on the reproductive fitness of competing parasite genotypes. We showed the existence of two basic response patterns--increase or decrease in reproductive fitness in multiple infections- depending on the parasite genotype. In all cases, the intensity of the response of any genotype depended on the genotype of the competing strain. This diversity of responses to multiple infections is probably maintained by the fluctuating frequencies of multiple infections in nature, arising from variations in disease pressure over the course of an epidemic and between successive epidemics. It allows a rapid response of parasitic populations to changing environments, which are particularly intense in agricultural systems.