The natural history of fig-pollinating wasps and their associated species-specific nematodes allows the measurement of many parameters which are relevant to testing hypotheses concerning host-parasite ecology and evolution. Within fig wasps species, it is possible to estimate lifetime reproductive success of foundress wasps as a function of presence or absence of nematode parasitism (virulence). Across species, there is a wide range of host population structures which, in turn, results in a range of opportunities for either horizontal or vertical nematode transmission. Therefore, estimates of virulence can be related to opportunities for transmission across a group of closely related hosts and their parasites. Further, the dynamics of the nematode infections over ecological and short-term evolutionary timescales can be monitored, giving added insight into the interpretation of the virulence estimates. Moreover, several scales of longer term evolutionary relationships are either known directly from fossil evidence or can be inferred from molecular data, providing deeper temporal context for the observed patterns. This combination of attributes permits detailed testing of hypotheses concerning the factors that potentially influence the evolution of virulence in host-parasite systems, and further, population and simulation models of the system that incorporate the parameter estimates can clarify the interpretation of how those factors act. There is little evidence suggesting that intermediate and long-term evolutionary relationships explain current levels of virulence. That is, it appears that virulence can change rapidly relative to speciation events, and that the nematodes do not tend to become ‘benign over time’. Instead, it appears that host population structure can influence the evolution of parasite virulence by affecting the relative opportunities for horizontal to vertical transmission, which, in turn, influences the relative costs and benefits of virulence to the nematodes. At one level, increased opportunities for horizontal transmission decouple the reproductive interests of the individual nematodes from those of the individual hosts that they are directly parasitizing, thereby reducing the cost of virulence to individual nematodes. At another level, increased opportunities of horizontal transmission also increases the relative frequency of hosts infected by multiple strains of nematodes. This promotes the evolution of more virulent forms by increasing the relative importance of within-host competition among nematode strains, thereby favouring strains that ‘eat more host sooner’. An interesting property of the fig-nematode systems is that the proportion of infected hosts does not change dramatically through time. This finding implies that there can be considerable negative effects on survival of infected hosts in addition to the previously documented reductions in fecundity of infected foundresses, because the latter are insufficient to account for the observed stability of wasp infection rates.