Transcriptomic and metabolomic profiles were used to unravel drought adaptation mechanisms in wild emmer wheat (Triticum turgidum ssp. dicoccoides), the progenitor of cultivated wheat, by comparing the response to drought stress in roots of genotypes contrasting in drought tolerance. The differences between the drought resistant (R) and drought susceptible (S) genotypes were characterized mainly by shifts in expression of hormone-related genes (e.g., gibberellins, abscisic acid (ABA) and auxin), including biosynthesis, signalling and response; RNA binding; calcium (calmodulin, caleosin and annexin) and phosphatidylinositol signalling, in the R genotype. ABA content in the roots of the R genotype was higher in the well-watered treatment and increased in response to drought, while in the S genotype ABA was invariant. The metabolomic profiling revealed in the R genotype a higher accumulation of tricarboxylic acid cycle intermediates and drought-related metabolites, including glucose, trehalose, proline and glycine. The integration of transcriptomics and metabolomics results indicated that adaptation to drought included efficient regulation and signalling pathways leading to effective bio-energetic processes, carbon metabolism and cell homeostasis. In conclusion, mechanisms of drought tolerance were identified in roots of wild emmer wheat, supporting our previous studies on the potential of this genepool as a valuable source for novel candidate genes to improve drought tolerance in cultivated wheat.