Trans-host effects can alter the ecological and evolutionary dynamics of parasite and host populations. Here, we examine whether resource limitation within a parasite's natal host affects propagule size and influences parasite fitness in a new host. To alter resource competition, we infected caterpillars with 3 doses of the nematode Steinernema carpocapsae and harvested transmission-stage juveniles either early or late in the infection. We measured the size of these juveniles, and then we examined their ability to colonize and their sex ratio upon maturity in a new host. We found a trade-off between the cumulative number and size of nematodes emerging from a host. Emerging nematode size declined significantly over the time course of the infection, but dose had no significant effects. Larger, early emerging nematodes had greater success in colonizing a new host than smaller, later emerging nematodes, independently of whether they needed to locate the host. Furthermore, although early emerging nematodes resulted in an equal sex ratio in the new host, late emerging nematodes resulted in female-biased populations. These transmission and sex-ratio effects demonstrate that conditions in the natal host can affect parasite fitness, and they suggest that trans-host effects need to be more fully integrated into our studies of parasite populations.