Energetics may provide a useful currency for studying the ecology of parasite assemblages within individual hosts. Parasite assemblages may also provide powerful models to study general principles of ecological energetics. Yet there has been little ecological research on parasite-host energetics, probably due to methodological difficulties. However, the scaling relationships of individual metabolic rate with body or cell-size and temperature may permit us to tackle the energetics of parasite assemblages in hosts. This paper offers the foundations and initial testing of a metabolic theory of ecology (MTE) framework for parasites in hosts. I first provide equations to estimate energetic flux through observed parasite assemblages. I then develop metabolic-scaling theory for parasite abundance, energetics, and biomass in individual hosts. In contrast to previous efforts, the theory factors in both host and parasite metabolic scaling, how parasites use host space, and whether energy or space dictates carrying capacity. Empirical tests indicate that host energetic flux can set parasite carrying capacity, which decreases as predicted considering the scaling of host and parasite metabolic rates. The theory and results also highlight that the phenomenon of “energetic equivalence” is not an assumption of MTE, but a possible outcome contingent on how species partition resources. Hence, applying MTE to parasites can lend mechanistic, quantitative, predictive insight into the nature of parasitism and can inform general ecological theory.