Global climate changes increase the frequency and intensity of heavy precipitation events, which result in flooding or soil waterlogging. One way to overcome these low-oxygen stresses is via modifying the plant root system to improve internal aeration. Here, we used a comparative RNA-seq based transcriptomic approach to elucidate the molecular mechanisms of waterlogging-triggered root plasticity in mungbean (Vigna radiata), a major grain legume cultivated in Asia. Two mungbean varieties with contrasting waterlogging tolerance due to the plasticity of the root system architecture were subjected to short-term and long-term waterlogging. Then, RNA-seq was performed. Genes highly expressed in both genotypes under short-term waterlogging are related to glycolysis and fermentation. Under long-term waterlogging, the expression of these genes was less induced in the tolerant variety, suggesting it had effectively adapted to waterlogging via enhancing root plasticity. Remarkably, under short-term waterlogging, the expression of several transcription factors that serve as integrators for ethylene and jasmonic acid signals controlling root stem cell development was highly upregulated only in the tolerant variety. Sequentially, root development-related genes were more expressed in the tolerant variety under long-term waterlogging. Our findings suggest that ethylene and jasmonic acids may contribute to waterlogging-triggered root plasticity by relaying environmental signals to reprogram root regeneration. This research provides the basis for the breeding and genetic engineering of waterlogging-tolerant crops in the future.