Mycorrhizosphere microbes enhance functioning of the plant–soil interface, but little is known of their ecology. This study aims to characterize the ascomycete communities associated with ectomycorrhizas in two Tasmanian wet sclerophyll forests. We hypothesize that both the phyto- and mycobiont, mantle type, soil microbiotope and geographical distance affect the diversity and occurrence of the associated ascomycetes. Using the culture-independent rDNA sequence analysis, we demonstrate a high diversity of these fungi on different hosts and habitats. Plant host has the strongest effect on the occurrence of the dominant species and community composition of ectomycorrhiza-associated fungi. Root endophytes, soil saprobes, myco-, phyto- and entomopathogens contribute to the ectomycorrhiza-associated ascomycete community. Taxonomically these Ascomycota mostly belong to the orders Helotiales, Hypocreales, Chaetothyriales and Sordariales. Members of Helotiales from both Tasmania and the Northern Hemisphere are phylogenetically closely related to root endophytes and ericoid mycorrhizal fungi, suggesting their strong ecological and evolutionary links. Ectomycorrhizal mycobionts from Australia and the Northern Hemisphere are taxonomically unrelated to each other and phylogenetically distant to other helotialean root-associated fungi, indicating independent evolution. The ubiquity and diversity of the secondary root-associated fungi should be considered in studies of mycorrhizal communities to avoid overestimating the richness of true symbionts.