TaWD40D that encodes a member of WD40 family proteins is a novel gene involved in the wheat response to abiotic stress. TaWD40D functions as a positive regulator of plant responses to salt stress and osmotic stress in plant. Abiotic stresses can severely affect plant growth and crop productivity. WD40 repeat-containing proteins play a key role in protein-protein or protein-DNA interactions by acting as scaffolding molecules and promoting protein activity. In this study, a stress-inducible gene, TaWD40D, was identified from Chinese spring wheat (Triticum aestivum L.). TaWD40D encodes a protein containing seven WD40 domains. Subcellular localization in Nicotiana benthamiana mesophyll cells and Arabidopsis root cells showed the presence of TaWD40D in the cytoplasm and nucleus. Heterologous overexpression of TaWD40D in Arabidopsis greatly increased plant tolerance to abscisic acid (ABA), salt stress, and osmotic stress during seed germination and seedling development. The expression patterns of two genes from the SOS pathway (SOS2 and SOS3) and three ABA genes (ABI2, RAB18 and DREB2A) functioning in ABA-dependent and ABA-independent pathways were altered in the transgenic lines overexpressing TaWD40D under the treatments. Notably, the basal level of the ABI2 expression was substantially increased in the TaWD40D overexpression lines. The down-regulation of TaWD40D in wheat by virus-induced gene silencing resulted in a decreased relative water content and less vigorous growth compared to non-silenced lines. Our results suggest that TaWD40D functions as a positive regulator of plant responses to salt stress and osmotic stress that could be utilized for the genetic improvement of stress tolerance in crop plants.