Linking characteristics of parasites to host diet-induced shifts in host-parasite interactions is a critical step in predicting the abundance of specific parasites within an ecosystem. A parasite’s infection route reflects a suite of parasite characteristics that could mediate the effects of host diet quality on host-parasite interactions, but the effect of infection route on the response of host-parasite interactions to host diet quality has not been quantified. We quantified these effects for the first time by experimentally manipulating a parasite capable of transmitting itself via multiple pathways utilized by a wide variety of parasites. We altered the diet phosphorus (P) content of Daphnia infected by the mixed mode transmitter Hamiltosporidian tvaerminnensis via one of two infection routes: horizontal, via the ingestion of spores from dead hosts, or vertical, via the infection of host offspring. Then, we quantified the effect of infection route on host diet-induced shifts in parasite load and virulence (i.e. host fecundity and survival). Overall, we found that horizontal infections were more sensitive to host diet than vertical infections. Low P diets decreased the parasite load and fecundity of all hosts, but had stronger negative effects on the loads of horizontally infected individuals than vertically infected ones. Likewise, horizontal infection reduced the survival of hosts fed low P (but not high P) diets while vertical infection did not affect survival. This increased sensitivity of horizontal infections to diet quality empirically supports the intuitive hypothesis that host diet quality exerts stronger effects on parasites that transmit via ingestion into a host’s gut than on parasites that transmit via routes less directly related to host nutrient uptake. Through these effects, host diet quality may shape the ecology and evolution of parasite communities.