The association between hosts and parasites results in reciprocal selective pressures over coevolutionary time. Over shorter ecological time scales, this is manifested by the negative impact of fitness-reducing parasites on host populations, and the positive effect of host density on parasite transmission and abundance. We use a large database on the densities and biomasses of all free-living and parasitic metazoans from multiple New Zealand lake ecosystems to address these reciprocal effects between hosts and parasites. First, we show that the bottom-up coupling of resource and consumer abundance predicted by ecological and epidemiological theory is evident, as seen by the positive relationship between parasite densities and those of their hosts across localities, independently of host and parasite taxa or modes of infection. From an energetic perspective, host populations appear undersaturated with parasites: parasite biomass scales with host biomass with a lower slope than predicted by theory. Second, we observed that across host populations, the variance in host density across a set of samples scales positively with mean density, following Taylor’s power law. However, the slope of this relationship differs between free-living taxa that are not parasitized and those that are parasitized. This suggests that parasitism exerts measurable effects on host population dynamics. Finally, the extent to which different parasite species achieve their highest abundance in the same localities is strongly dependent on similarities in life cycles: the more intermediate and definitive hosts are shared between two parasites, the stronger the spatial covariance in their local abundances. Thus, some host populations are more likely than others to suffer additive or synergistic effects from multiple parasites. The strength of the population regulation and selective pressure exerted by parasites on their hosts is therefore measurable across a broad spectrum of taxa, and structured spatially with multiple parasite species sharing hotspots of infection.