A key trait conferring flood tolerance is the ability to grow adventitious roots as a response to submergence. The genetic traits of deepwater rice determining the development and characteristics of aquatic adventitious roots (AAR) had not been evaluated. We used near-isogenic lines introgressed to test the hypothesis that the impressive shoot elongation ability of deepwater rice linked to quantitative trait loci 1 and 12 also promote the development of AAR. The deepwater rice genotype NIL-12 possessed expanded regions at the stem nodes where numerous AAR developed as a response to submergence. Two types (AR1 and AR2) of roots with distinct timing of emergence and large differences in morphological and anatomical traits formed within 3 (AR1) to 7 (AR2) d of submergence. The mechanical impedance provided by the leaf sheath caused AR2 to emerge later promoting thicker roots, higher elongation capacity and higher desiccation tolerance. Upregulation of key genes suggests a joint contribution in activating the meristem in AAR enhancing the development of these in response to submergence. The morphological and anatomical traits suggested that AR2 is better adapted to long-term flooding than AR1. We therefore propose that AR2 in deepwater rice functions as an evolutionary defence strategy to tackle periodic submergence.