Lodgepole pine forests are under threat due to wildfires of increasing severity and frequency coupled with tree mortality from insect outbreaks. Soil microbial communities, which drive biogeochemical cycles and partner in mycorrhizal symbiosis with lodgepole pines, play critical roles in the ability of these forests to survive and regenerate in the face of simultaneous global change threats. How soil microbial communities are influenced by fire severity and soil depth and how they recover over time in lodgepole pine forests with existing insect-driven mortality remains an open question. Here, we sampled two soil depths (0–5 and 5–15 cm) and various burn severities across a ten-year wildfire chronosequence in the Southern Rocky Mountains. We used qPCR of 18S and 16S rRNA genes to assess changes in fungal and bacterial abundance and ITS2 and 16S amplicon sequencing to assess fungal and bacterial richness and composition. Our results show that: 1) higher severity fires led to larger reductions of both fungal and bacterial abundance and richness, 2) the impact of fire on fungal and bacterial communities was modulated by soil depth, with more severe impacts in shallower soils 3) both fungal and bacterial communities exhibit a partial recovery of abundance and species richness in older fires, 4) fire severity is the main driver of fungal and bacterial community structure but its effect varied across time, 5) pyrophilous “fire-loving” fungi and bacteria exhibit an increased abundance in burned plots, particularly in recent fires, and 6) symbiotic ectomycorrhizal fungi are particularly hard hit by the compound effect of the beetle-driven tree mortality and wildfires. They exhibit a consistently low abundance and richness in the high severity plots which did not recover over time, and unburned plots have a depauperated ectomycorrhizal community.