Wild and weedy relatives of domesticated plants contain genetic variants that can be beneficial for crop improvement through agricultural biotechnology. Through comparisons of the responses of wild ancestors and cultivars to abiotic stress, important information for targeted plant breeding can be obtained. Here, wild ancestral green foxtail (GWC) and two foxtail millet cultivars (landrace Qitoubai, QG, and modern cultivar Jingu21, G21) were selected to detect different responses to drought stress at the 6-leaf stage. The results showed that drought resulted in the largest decrease in biomass in the G21 (57.3%) compared with 53.2% and 32.5% in QG and GWC, respectively. The cultivar G21 exhibited the highest whole plant transpiration and root exudation index under drought conditions, followed by QG and then GWC. Under drought stress, abscisic acid (ABA) content was the highest in GWC followed by QG and G21. Two genes involved in the ABA pathway were downregulated in G21 plants, but not in GWC and QG plants under drought stress. The expression of the β-amylase and SWEET gene was upregulated by drought stress in landrace and green foxtail, whereas the expression was less affected in the modern cultivar, which could contribute to a higher non-structural carbon content. Overexpression of β-amylase in Arabidopsis thaliana (OE) increased OE plant biomass significantly, showing that β-amylase could be involved in adapting to drought in foxtail. Taking together, the smaller increase in drought-induced ABA content and decreased ABA response induced high leaf transpiration, which provided a strong transpiration pull, increasing root water uptake and root absorption capacity, thereby resulting in low soil water content in G21. The higher non-structural carbon content provided more osmotic regulatory substances, helping to maintain water status in leaves of GWC. These data can be used to inform future plant breeding efforts aimed at further improving drought resistance in important grain crops.