Wild relatives of wheat have served as a pool of genetic variation for understanding salinity tolerance mechanisms. Two separate experiments were performed to evaluate the natural diversity in root and shoot Na exclusion and K accumulation, and the activity of four antioxidant enzymes within an extensive collection of ancestral wheat accessions. In the initial screening experiment, salinity stress (300 mm NaCl) significantly increased Na concentration in roots and leaves and led to a significant decline in root and shoot fresh weights, dry weights, and K contents. Principal component analysis of the 181 accessions and 12 species identified three first components accounted for 63.47% and 78.55% of the variation under salinity stress. We identified 12 accessions of each species with superior tolerance to salinity for further assessment of their antioxidant defence systems in response to salinity. Both mild (250 mm NaCl) and severe (350 mm NaCl) levels of salinity significantly increased activities of four enzymes, indicating an enhanced antioxidant-scavenging system for minimising the damaging effects of H₂O₂. Some of the wild relatives—Aegilops speltoides (putative B genome), Ae. caudata (C genome), Ae. cylindrica (DC genome) and Triticum boeoticum (A^b genome)—responded to salinity stress by increasing antioxidants as the dominant mechanism to retain oxidative balance in cells. Further evaluation of salt-tolerance mechanisms in these superior wild relatives will help us to understand the potential of wheat progenitors in the development of more salt-tolerant varieties.