Rice (Oryza sativa L.) seedlings grown under nitrogen (N) deficiency conditions show a foraging response characterized by increased root length. However, the mechanism underlying this developmental plasticity is still poorly understood. In this study, the mechanism by which N deficiency influences rice seminal root growth was investigated. The results demonstrated that compared with the control (1 mM N) treatment, N deficiency treatments strongly promoted seminal root growth. However, the N deficiency-induced growth was negated by the application of zeatin, which is a type of cytokinin (CK). Moreover, the promotion of rice seminal root growth was correlated with a decrease in CK content, which was due to the N deficiency-mediated inhibition of CK biosynthesis through the down-regulation of CK biosynthesis genes and an enhancement of CK degradation through the up-regulation of CK degradation genes. In addition, the N deficiency-induced decrease in CK content not only enhanced the root meristem cell proliferation rate by increasing the meristem cell number via the down-regulation of OsIAA3 and up-regulation of root-expressed OsPLTs, but also promoted root cell elongation by up-regulating cell elongation-related genes, including root-specific OsXTHs and OsEXPs. Taken together, our data suggest that an N deficiency-induced decrease in CK content promotes the seminal root growth of rice seedlings by promoting root meristem cell proliferation and cell elongation.