Warmer climates are already contributing to significant decreases in wheat (Triticum spp.) yields worldwide, highlighting the need for more adapted germplasm. Although many studies have addressed the effects of warmer climates on grain physiology and photosynthesis, only a few have considered temperature effects on other key yield-related traits such as the sensitivity of transpiration rate (TR) to vapour pressure deficit (VPD) − a function of air temperature and relative humidity. In wheat, no reports are available to document such influences. More importantly, the relative contributions of heat-stress night and day conditions on such sensitivity and the plant’s evaporative surface remain to be investigated. The objective of this study was to assess the response of these two physiological processes to long-term (i.e. 3 weeks) exposures to six warming scenarios, consisting of a combination of three target growth-period VPD (2, 2.7 and 4 kPa), and two night temperature (20 and 30°C) regimes among 11 diverse bread and durum wheat lines having different origins. The study revealed (i) a large genetic variability in those responses; (ii) non-linear interactions between the effects of day and night conditions; and (iii) compensation mechanisms between leaf areas and transpiration sensitivities to VPD together with differential acclimation strategies of these sensitivities with respect to increasingly warmer scenarios. These findings open the way to implementing breeding strategies that can improve wheat yields under different warming scenarios.