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 that R_d and Rubisco carboxylation capacity (V_cmax) at 25°C (R_d,25, V_cmax,25) are coordinated so that R_d,25 variations support V_cmax,25 at a level allowing full light use, with V_cmax,25 reflecting daytime conditions (for photosynthesis), and R_d,25/V_cmax,25 reflecting 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,25 declines linearly with daily average prior temperature; R_d at average prior night temperatures tends towards a constant value; and R_d,25/V_cmax,25 is constant. Our hypothesis accounted for more variation in observed R_d,25 over time (R² = 0.74) and space (R² = 0.68) than the alternatives. Night‐time temperature dominated the seasonal time‐course of R_d, with an apparent response time scale of c. 2 wk. V_cmax dominated the spatial patterns. Our acclimation hypothesis results in a smaller increase in global R_d in response to rising CO₂ and warming than is projected by the two of three alternative hypotheses, and by current models.