Adventitious roots in canopy soils associated with silver beech (Nothofagus menziesii Hook.f. (Nothofagaceae)) form ectomycorrhizal associations. We investigated the extent to which canopy ectomycorrhizal communities contribute to overall diversity of ectomycorrhizal fungi associated with silver beech. Hyphal ingrowth bags were buried for 12 months in canopy and terrestrial soils of five trees at one site. We used amplicon sequencing of the nuclear ribosomal internal transcribed spacer 2 region (ITS2) to assess diversity of both ectomycorrhizal and non-ectomycorrhizal OTUs in hyphal ingrowth bags. There was a significant difference in ectomycorrhizal fungal community diversity between the terrestrial and canopy hyphal ingrowth bag communities. Ectomycorrhizal community composition of the terrestrial and canopy environments was also significantly different. Some ectomycorrhizal taxa were significantly differentially represented in either the terrestrial or canopy environment. The hyphal ingrowth bags also accumulated non-ectomycorrhizal species. The non-ectomycorrhizal fungi also had significantly different diversity and community composition between the canopy and terrestrial environments. Like the ectomycorrhizal community, some non-ectomycorrhizal taxa were significantly differentially represented in either the terrestrial or canopy environment. The canopy soil microhabitat provides a novel environment for growth of ectomycorrhizal adventitious roots and enables the spatial partitioning of ectomycorrhizal and non-ectomycorrhizal fungal diversity in the forest.