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Summary Leaf dark respiration (R_d) acclimates to environmental changes. However, the magnitude, controls and time scales of acclimation remain unclear and are inconsistently treated in ecosystem models.We hypothesized thatR_dand Rubisco carboxylation capacity (V_cmax) at 25°C (R_d,25,V_cmax,25) are coordinated so thatR_d,25variations supportV_cmax,25at a level allowing full light use, withV_cmax,25reflecting daytime conditions (for photosynthesis), andR_d,25/V_cmax,25reflecting night‐time conditions (for starch degradation and sucrose export). We tested this hypothesis temporally using a 5‐yr warming experiment, and spatially using an extensive field‐measurement data set. We compared the results to three published alternatives:R_d,25declines linearly with daily average prior temperature;R_dat average prior night temperatures tends towards a constant value; andR_d,25/V_cmax,25is constant.Our hypothesis accounted for more variation in observedR_d,25over time (R² = 0.74) and space (R² = 0.68) than the alternatives. Night‐time temperature dominated the seasonal time‐course ofR_d, with an apparent response time scale ofc.2 wk.V_cmaxdominated the spatial patterns.Our acclimation hypothesis results in a smaller increase in globalR_din response to rising CO₂and warming than is projected by the two of three alternative hypotheses, and by current models.