Classic ectomycorrhizal symbioses are mutualisms that involve the exchange of fixed carbon for mineral nutrients between plant roots and fungi. They are unique in the way they contain features of both intimate and diffuse symbioses. The degree of host specificity varies, particularly among the fungi. Here we examine two exceptional cases of specificity to see what they tell us about the advantages of specificity, how it is initiated, and the potential role that it plays in complex ecosystems. The first case involves non-photosynthetic epiparasitic plants, which contrary to virtually all other plants, exhibit high levels of specificity toward their fungal hosts. The second case involves suilloid fungi; this is the largest monophyletic group of ectomycorrhizal fungi that is essentially restricted to associations with a single plant family. In both cases, new symbioses are initiated by dormant propagules that are stimulated to germinate by chemical cues from the host. This reduces the cost of wasting propagules on non-hosts. The advantages of specificity remain unclear in both cases, but we argue that increased benefit to the specialist may result from specialized physiological adaptations. We reexamine the idea that specialist fungi may help their hosts compete in complex ecosystems by reducing facultative epiparasitism by other plants, and suggest an alternative hypothesis for the observed pattern.