Soil fungal communities are vital for post-fire ecosystem restoration because of their ability to cycle nutrients and form symbiotic partnerships with regenerating trees. However, understanding is limited about how high-severity wildfires influence the fungal community of ecosystems adapted to low-severity fires. We studied an 11-year-old chronosequence of high-severity burn ponderosa pine (Pinus ponderosa) in eastern Washington, USA. Using Illumina MiSeq of the ITS1, we examined changes in soil nutrients, drivers of ectomycorrhizal (EcM) and saprobic fungal richness, community shifts, and post-fire fungal succession. High-severity wildfires reduced EcM fungal richness by an average of 45.8% and saprobic richness by 11.7%, leading to significant, long-term alterations to the post-fire fungal communities that did not return to unburned levels even after 11 years. Over time, differences in the post-fire fungal community were driven by the dominance of several pyrophilous fungi, including the EcM Ascomycete genera Pustularia and Wilcoxina, and the saprobic Basidiomycete genus Geminibasidium, which decreased in abundance with time post-fire. EcM fungi and saprobes were intimately linked to the soil environment: total carbon, total nitrogen, and their interaction with fire predicted ectomycorrhizal richness, while total carbon, time since fire, and the interaction between time since fire and treatment predicted saprobic species richness. We conclude that high-severity wildfires reduced EcM richness and significantly altered the EcM and saprobic fungal communities of this fire-adapted ecosystem, selecting resilient and fire-adapted species, such as W. rehmii and Geminibasidium sp., thus initiating post-fire succession.