The heterogeneity of cell-types in plant roots provides the structural and mechanistic basis for root responses to developmental and environmental signals, including the availability of the major mineral nutrient nitrogen (N) in the soil. To date, single-cell-resolution analyses of transcriptional responses to external nitrogen supply remain limited in plant and crop species. Here, we performed single-cell multiomic profiling of tomato (Solanum lycopersicum) roots treated with different nitrogen conditions, generating a high-resolution map of root responses to environmental nitrogen availability. We identified root cell types important for nitrogen response, discovered transcriptional regulators and nitrogen-responsive genes in a cell-type-specific manner, and generated a gene regulatory network across nitrogen conditions that can be used to investigate transcriptional circuits in specific cell types. This single-cell-resolution nitrogen-responsive map of the tomato roots provides a valuable knowledge base for identifying candidate genes to improve nitrogen use efficiency in horticultural crop species.