Background: Compartmentalization and nestedness are common patterns in ecological networks. The aim of this study was to elucidate some of the processes shaping these patterns in a well resolved network of host/pathogen interactions. Methology/Principal Findings: Based on a long-term (1972–2005) survey of forest health at the regional scale (all French forests; 15 million ha), we uncovered an almost fully connected network of 51 tree taxa and 157 parasitic fungal species. Our analyses revealed that the compartmentalization of the network maps out the ancient evolutionary history of seed plants, but not the ancient evolutionary history of fungal species. The very early divergence of the major fungal phyla may account for this asymmetric influence of past evolutionary history. Unlike compartmentalization, nestedness did not reflect any consistent phylogenetic signal. Instead, it seemed to reflect the ecological features of the current species, such as the relative abundance of tree species and the life-history strategies of fungal pathogens. We discussed how the evolution of host range in fungal species may account for the observed nested patterns. Conclusion/Significance: Overall, our analyses emphasized how the current complexity of ecological networks results from the diversification of the species and their interactions over evolutionary times. They confirmed that the current architecture of ecological networks is not only dependant on recent ecological processes.