ZD958 was the most low-N-efficient line among five maize and two teosinte lines. Zea parviglumis and Zea diploperennis were insensitive to N limitation. Maize and teosinte genetically and evolutionarily diverged in gene regulation. GDH2, ASN2, and T4 were consistently down-regulated across seven lines. Maternal asymmetric inheritance and heterosis vigor made ZD958 low-N-efficient. Nitrogen (N) deficiency remains a serious limiting factor for maize production in many developing countries. It is particularly important to better understand how hybrid maize responds to N limitation. ZD958, a dominant high-yield hybrid in North China, was comparatively analyzed with four other maize and two teosinte lines at physiological and transcriptional levels. ZD958 was the most low-N-efficient line among five maize and two teosinte lines due to its largest biomass accumulation at a lowest N concentration under N limitation; while Zea parviglumis and Zea diploperennis had large root systems and were insensitive to N limitation. In anti-parallel with down-regulation of N metabolic genes in the ZD958 root, carbon allocation towards the root was enhanced for the significant increase in the root length. Variations in expression patterns of ten genes mediating N uptake, transport, and metabolism indicated large genetic and evolutionary divergence among seven lines under N limitation. Notably, GDH2, ASN2, and VAAT5 were consistently down-regulated under N limitation across these maize and teosinte lines, suggesting essential evolutionary conservation of gene regulation in response to N limitation and providing molecular markers for N nutritional diagnosis. Asymmetric inheritance, mostly from its maternal donor Z58, and heterosis vigor made ZD958 low-N-efficient at the seedling stage. The superior traits in crown roots in ZD958 may be derived from its paternal donor Chang7-2. Thus, Z58, Chang7-2, and two wild maize lines (Z. parviglumis and Z. diploperennis) provide valuable germplasms for N-efficient and large-root maize breeding.