Gas exchange, growth, water transport and carbon (C) metabolism diminish during drought according to their respective sensitivities to declining water status. The timing of this sequence of declining physiological functions may determine how water and C relations compromise plant survival. In this paper, we test the hypothesis that the degree of asynchrony between declining C supply (photosynthesis) and C demand (growth and respiration) determines the rate and magnitude of changes in whole-plant non-structural carbohydrates (NSC) during drought. Two complementary experiments using two tree species (Eucalyptus globulusLabill. andPinus radiataD. Don) with contrasting drought response strategies were performed to (i) assess changes in radial stem growth, transpiration, leaf water potential and gas exchange in response tochronicdrought, and (ii) evaluate the concomitant impacts of these drought responses on the temporal patterns of NSC duringterminaldrought. The three distinct phases of water stress were delineated by thresholds of growth cessation and stomatal closure that defined the ‘carbon safety margin’ (i.e., the difference between leaf water potential when growth is zero and leaf water potential when net photosynthesis is zero). A wider C safety margin inE. globuluswas defined by an earlier cessation of growth relative to photosynthesis that reduced the demand for NSC while maintaining C acquisition. By contrast, the narrower C safety margin inP. radiatawas characterized by a synchronous decline in growth and photosynthesis, whereby growth continued under a declining supply of NSC from photosynthesis. The narrower C safety margin inP. radiatawas associated with declines in starch concentrations after ∼90 days ofchronicdrought and significant depletion of starch in all organs at mortality. The observed divergence in the sensitivity of drought responses is indicative of a potential trade-off between maintaining hydraulic safety and adequate C availability.