Beech (Fagus sylvatica), a dominant forest species in Central Europe, competes for nitrogen with soil microbes and suffers from N limitation under dry conditions. We hypothesized that ectomycorrhizal communities and the free-living rhizosphere microbes from beech trees from sites with two contrasting climatic conditions exhibit differences in N acquisition that contribute to differences in host N uptake and are related to differences in host belowground carbon allocation. To test these hypotheses, young trees from the natural regeneration of two genetically similar populations, one from dryer conditions (located in an area with a southwest exposure [SW trees]) and the other from a cooler, moist climate (located in an area with a northeast exposure [NE trees]), were transplanted into a homogeneous substrate in the same environment and labeled with (13)CO2 and (15)NH4 (+). Free-living rhizosphere microbes were characterized by marker genes for the N cycle, but no differences between the rhizospheres of SW or NE trees were found. Lower (15)N enrichment was found in the ectomycorrhizal communities of the NE tree communities than the SW tree communities, whereas no significant differences in (15)N enrichment were observed for nonmycorrhizal root tips of SW and NE trees. Neither the ectomycorrhizal communities nor the nonmycorrhizal root tips originating from NE and SW trees showed differences in (13)C signatures. Because the level of (15)N accumulation in fine roots and the amount transferred to leaves were lower in NE trees than SW trees, our data support the suggestion that the ectomycorrhizal community influences N transfer to its host and demonstrate that the fungal community from the dry condition was more efficient in N acquisition when environmental constraints were relieved. These findings highlight the importance of adapted ectomycorrhizal communities for forest nutrition in a changing climate.