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Abstract Plant–mycorrhizal interactions mediate plant nitrogen (N) limitation and can inform model projections of the duration and strength of the effect of increasing CO₂on plant growth. We present dendrochronological evidence of a positive, but context-dependent fertilization response ofQuercus rubra L. to increasing ambient CO₂(iCO₂) along a natural soil nutrient gradient in a mature temperate forest. We investigated this heterogeneous response by linking metagenomic measurements of ectomycorrhizal (ECM) fungal N-foraging traits and dendrochronological models of plant uptake of inorganic N and N bound in soil organic matter (N-SOM). N-SOM putatively enhanced tree growth under conditions of low inorganic N availability, soil conditions where ECM fungal communities possessed greater genomic potential to decay SOM and obtain N-SOM. These trees were fertilized by 38 years of iCO₂. In contrast, trees occupying inorganic N rich soils hosted ECM fungal communities with reduced SOM decay capacity and exhibited neutral growth responses to iCO₂. This study elucidates how the distribution of N-foraging traits among ECM fungal communities govern tree access to N-SOM and subsequent growth responses to iCO₂.