Aegilops tauschii, as a donor of D genome to the bread wheat with a valuable source of resistance to different biotic and abiotic stresses, is used to improve the quality of wheat cultivars. Every genotype has a specific genetic content, the investigation of which can lead to the identification of useful genes such as stress tolerance genes, including drought. Therefore, 23 genotypes of Ae. tauschii were selected to evaluate their morphological and physiological traits under greenhouse conditions. Among them, a superior tolerant genotype (KC-2226) was chosen for transcriptomic analysis. Our result showed that 5007 and 3489 genes were deferentially up- and downregulated, respectively. Upregulated genes were involved in photosynthesis, glycolysis/gluconeogenesis, and amino acid biosynthesis whereas downregulated genes were often engaged in DNA synthesis, replication, repair and topological changes. The result of protein–protein interaction network analysis showed that AT1G76550 (1.46), AT1G20950 (1.42), IAR4 (1.19), and PYD2 (1.16) among upregulated genes and THY-1 (44), PCNA1 (41) and TOPII (22) among down-regulated genes had the highest interactions with other genes. In conclusion, Ae. tauschii employs elevated transcription of specific genes involved in photosynthesis, glycolysis and gluconeogenesis and amino acid biosynthesis pathways rather than genes active in DNA synthesis and repair to provide the energy needed for the plant to survive under stress conditions.