Terrestrial biosphere models (TBMs) disagree on how the terrestrial carbon sink responds to climate futures. On climate-change timescales, this response is primarily regulated by the competing responses of photosynthetic carbon uptake to increasing CO₂ and respiratory carbon loss to increasing temperature, among others. Whereas emerging photosynthetic proxies bring about increasingly robust biome-scale constraints on photosynthetic responses, the response of respiration to climate remains highly uncertain due to the lack of observational constraints directly informing biome-scale responses. Here, we leverage in situ atmospheric CO₂ observations from a network of tall towers over North America and estimates of ecosystem respiration from an ensemble of TBMs and data-driven models to derive the biome-scale temperature sensitivity of ecosystem respiration. We find that a large subset of models shows higher biome-scale temperature sensitivities of ecosystem respiration than atmospheric observations suggest. We further show that correcting the temperature sensitivity of ecosystem respiration improves these models’ ability to explain observed atmospheric CO₂ variability. This inconsistency between bottom-up representations of respiratory processes and the observed overall biome-scale responses highlights an urgent need to evaluate parameterizations of respiratory processes directly on biome scales, leveraging top-down observational constraints. Given the lower biome-scale temperature sensitivity of ecosystem respiration than those represented in a large subset of TBMs, the terrestrial carbon sink may be more resilient to warming than expected from model ensemble behavior.