Heterotrophic ammonia-oxidizing bacteria (HAOB), crucial for soil nitrification, have unclear benefits for crop water use. This study explored the impact of a novel HAOB strain, S2_8_1, on maize drought resilience via pot culturing. The experiment included various treatments: control with sufficient water (CK), sufficient water + HAOB strain (WI), limited rewatering (DL), sufficient rewatering (DH), sufficient rewatering + HAOB strain (DHI), and limited rewatering + HAOB strain (DLI). The results revealed below-compensatory growth with DL compared to CK. Interestingly, the HAOB strain displayed survival resilience with a 96% increase in its copy numbers in the rhizosphere soils compared to CK during rewatering. The DLI treatment exhibited equal to compensatory growth, showing a remarkable 169% surge in the water use efficiency versus CK. This improvement was attributed to heightened rhizosphere soil nitrification by HAOB, enhancing the cytokinin production in roots and its transference to leaves, leading to a 25% higher leaf cytokinin concentration with DLI compared to CK during rewatering. Additionally, HAOB DHI prompted overcompensatory growth after sufficient rewatering, boosting nitrification and facilitating cytokinin root-to-leaf transport. However, its water use efficiency was 39% lower than DLI. The study highlights HAOB’s importance in optimizing crop water use, particularly in scenarios of limited rewatering in cropland soils.