Rising temperatures are a major threat to global wheat production, particularly when accompanied by other abiotic stressors such as mineral nutrient deficiencies. This study aimed to quantify the effects of supra-optimal temperature on growth, photosynthetic performance, and antioxidative responses in bread wheat cultivars grown under varied zinc (Zn) supply. Two bread wheat cultivars (Triticum aestivum L., cvs. Lasani-2008 and Faisalabad-2008) with varied responsiveness to Zn supply and drought tolerance were cultured in nutrient solution with low (0.1 µM) or adequate (1.0 µM) Zn under optimal (25/20°C day/night) or supra-optimal (36/28°C day/night) temperature regimes. Supra-optimal temperature severely reduced root but not shoot biomass, whereas low Zn reduced shoot as well as root biomass. Shoot-to-root biomass ratio was reduced under low Zn but increased under supra-optimal temperature. Supra-optimal temperature inhibited root elongation and volume particularly in plants supplied with low Zn. In both cultivars, Zn efficiency index was reduced by supra-optimal temperature, whereas heat tolerance index was reduced by low Zn supply. Supra-optimal temperature decreased photosynthesis, quantum yield, and chlorophyll density in low-Zn but not in adequate-Zn plants. In comparison, low Zn decreased specific activities of superoxide dismutase (SOD) and ascorbate peroxidase (APX) and increased glutathione reductase (GR), where supra-optimal temperature increased SOD, decreased GR and did not change APX activity in leaves and roots. Moreover, supra-optimal temperature severely reduced shoot Zn concentration and Zn uptake per plant specifically under adequate Zn supply. Overall, supra-optimal temperature exacerbated adverse effects of low Zn supply, resulting in severe reductions in growth traits viz. shoot and root biomass, root length and volume, and consequently impeded Zn uptake, enhanced oxidative stress and impaired photosynthetic performance. Adequate Zn nutrition is crucial to prevent yield loss in wheat cultivated under supra-optimal temperatures.