Mixed-genotype infections have attracted considerable attention as drivers of pathogen evolution. However, experimental approaches often overlook essential features of natural host-parasite interactions, such as host heterogeneity, or the effects of between-host selection during transmission. Here, following inoculation of a mixed infection, we analyse the success of different strains of a trypanosome parasite throughout the colony cycle of its bumblebee host. We find that most colonies efficiently filter the circulating infection before it reaches the new queens, the only offspring that carry infections to the next season. A few colonies with a poor filtering ability thus contributed disproportionately to the parasite population in the next season. High strain diversity but not high infection intensity within colony was associated with an increased probability of transmission of the infection to new queens. Interestingly, the representation of the different strains changed dramatically over time, so that long-term parasite success could not be predicted from short-term observations. These findings highlight the shaping of within-colony parasite diversity through filtering as a crucial determinant of year-to-year pathogen transmission and emphasize the importance of host ecology and heterogeneity for disease dynamics.