Summary Identifying the potential for natural soil microbial communities to predictably affect complex plant traits is an important frontier in climate change research. Plant phenology varies with environmental and genetic factors, but few studies have examined whether the soil microbiome interacts with plant population differentiation to affect phenology and ecosystem function. We compared soil microbial variation in a widespread tree species (Populus angustifolia) with different soil inoculum treatments in a common garden environment to test how the soil microbiome affects spring foliar phenology and subsequent biomass growth. We hypothesized and show that soil bacterial and fungal communities vary with tree conditioning from different populations and elevations, that this soil community variation influences patterns of foliar phenology and plant growth across populations and elevation gradients, and that transferring lower elevation plant genotypes to higher elevation soil communities delayed foliar phenology, thereby shortening the growing season and reducing annual biomass production. Our findings show the importance of plant–soil interactions that help shape the timing of tree foliar phenology and productivity. These geographic patterns in plant population × microbiome interactions also broaden our understanding of how soil communities impact plant phenotypic variation across key climate change gradients, with consequences for ecosystem functioning.