Previous studies have suggested that the maintenance of redox homeostasis is essential for plant growth. Here we investigated how redox homeostasis and signalling is modulated in response to different nitrogen (N) forms in tea plant roots. Our results showed that both N deficiency and nitrate (NO3-) can trigger the production of hydrogen peroxide and lipid peroxidation in roots. In contrast, these responses were not altered by NH4+. Further, N deficiency and NO3--triggered redox imbalance was re-established by increased of proanthocyanidins (PAs) and glutathione (GSH), as well as upregulation of representative antioxidant enzyme activities and genes. To further explore the molecular bases of these responses, comparative transcriptome analysis was performed, and redox homeostasis-associated differentially expressed genes (DEGs) were selected for bioinformatics analysis. Most of these genes were involved in the flavonoid biosynthesis, GSH metabolism and the antioxidant system, which was specifically altered by N deficiency or NO3-. Moreover, the interplay between H2O2 (generated by RBOH and Ndufab1) and hormones (including abscisic acid, auxin, cytokinin and ethylene) in response to different N forms was suggested. Collectively, the above findings contribute to an understanding of the underlying molecular mechanisms of redox homeostasis and signalling in alleviating oxidative stress in tea plant roots.