Nonmycorrhizal root-colonizing fungi are key determinants of plant growth, driving processes ranging from pathogenesis to stress alleviation. Evidence suggests that they might also facilitate host access to soil nutrients in a mycorrhiza-like manner, but the extent of their direct contribution to plant nutrition is unknown. To study how widespread such capacity is across root-colonizing fungi, we surveyed soils in nutrient-limiting habitats using plant baits to look for fungal community changes in response to nutrient conditions. We established a fungal culture collection and used Arabidopsis thaliana inoculation bioassays to assess the ability of fungi to facilitate host’s growth in the presence of organic nutrients unavailable to plants. Plant baits captured a representation of fungal communities extant in natural habitats and showed that nutrient limitation has little influence on community assembly. Arabidopsis thaliana inoculated with 31 phylogenetically diverse fungi exhibited a consistent fungus-driven growth promotion when supplied with organic nutrients compared to untreated plants. However, direct phosphorus measurement and RNA-seq data did not support enhanced nutrient uptake but rather that growth effects may result from changes in the plant’s immune response to colonization. The widespread and consistent host responses to fungal colonization suggest that distinct, locally adapted nonmycorrhizal fungi affect plant performance across habitats.