Plants associating with mutualistic ectomycorrhizal (ECM) fungi may directly obtain nitrogen (N) bound in soil organic matter (N-SOM). However, the contribution of N-SOM to plant growth under field conditions remains poorly constrained. We tested the hypothesis that turnover in ECM communities along soil inorganic N gradients mediates a functional transition from plant reliance on N-SOM in low inorganic N soils, to primarily inorganic N uptake in inorganic N-rich condition soils. We quantified the δ 15 N of Q. rubra foliage and roots, organic and inorganic soil N pools, and used molecular sequencing to characterize ECM communities, morpho-traits associated with N-foraging, and a community aggregated sporocarp δ 15 N. In support of our hypothesis, we document the progressive enrichment of root and foliar δ 15 N with increasing soil inorganic N supply; green leaves ranged from − 5.95 to 0.16‰ as the supply of inorganic N increased. ECM communities inhabiting low inorganic N soils were dominated by the genus Cortinarius, and other fungi forming hyphal morphologies putatively involved in N-SOM acquisition; sporocarp estimates from these communities were enriched (+ 4‰), further supporting fungal N-SOM acquisition. In contrast, trees occurring in high inorganic N soils hosted distinct communities with morpho-traits associated with inorganic N acquisition and depleted sporocarps (+ 0.5‰). Together, our results are consistent with apparent tradeoffs in the foraging cost and contribution of N-SOM to plant growth and demonstrate linkages between ECM community composition, fungal N-foraging potential and foliar δ 15 N. The functional characteristics of ECM communities represent a mechanistic basis for flexibility in plant nutrient foraging strategies. We conclude that the contribution of N-SOM to plant growth is likely contingent on ECM community composition and local soil nutrient availability.