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Wildfires are important natural disturbances with profound ecological impacts. However, our understanding of how to restore plant–soil microbiome interactions following wildfires remains limited, revealing a key knowledge gap in post‐wildfire ecosystem restoration. To assess the restoration of plant‐microbiome interactions in fire‐affected ecosystems, we conducted greenhouse experiments simulating wildfire effects on soil collected from Maulino Coastal Forest of central Chile, a biodiversity hotspot. We measured the plant height and photosynthesis over 90 days, and two‐year survival probability, of three common native (Aristotelia chilensis, Nothofagus glauca and N. alessandrii) and three non‐native species (Eucalyptus globulus, Pinus radiata and Genista monspessulana) planted in three soils (unburned, burned and burned soil inoculated with the native microbiome). Available nutrient concentrations (N, P and K) and activities of microbial enzymes (dehydrogenase, β‐glucosidase and urease) were also measured over 360 days. Available nutrient concentrations were consistently higher in burned and burned‐inoculated soils than in unburned soils. Enzyme activities in unburned and burned‐inoculated soils remained higher than in burned soil, indicating that the native microbiome restored microbial enzyme activities. The increase in height over 90 days was lower in burned soils compared with unburned soils for native species. However, inoculation with the native microbiome mitigated this negative effect, resulting in height increases similar to those in unburned soils. For non‐native species, burning and inoculation had negligible effects on the height increases. Similar patterns were observed for the increase in photosynthetic rate, with native species showing a reduced rate in burned soils, which was offset by microbiome inoculation, while non‐native species were unaffected by both treatments. Survival probability of native species declined in burned soil, but was the same in burned‐inoculated soil as in unburned soil. That of non‐native species was unaffected by burning or by inoculation with the native microbiome. Synthesis and applications. Native microbiomes are evidently promising tools to safeguard ecosystem functionality and mitigate species extinction risks arising from climate change and human‐induced wildfires. We advocate integrating microbiomes into future active restoration strategies for fire‐affected ecosystems. [ABSTRACT FROM AUTHOR]