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Carbon isotope records from alkenone biomarkers (ε_p37:2) produced by haptophyte algae are frequently used for atmospheric CO₂paleobarometry, but this method has yielded inconsistent results during periods where CO₂variations are known independently. Recent syntheses of algal cultures have quantitatively demonstrated that ε_p37:2indeed records CO₂information: ε_p37:2increases as aqueous CO₂concentrations increase relative to carbon demand. However, interpretations of ε_p37:2are complicated by irradiance, where higher irradiance yields higher ε_p37:2. Here we examine the roles of physiology and environment in setting ε_p37:2in the ocean. We compile water‐column and sediment core‐top ε_p37:2data and add new core‐top measurements, including estimates of cell sizes and growth rates of the alkenone‐producing population. In support of culture studies, we find irradiance to be a key control on ε_p37:2in the modern ocean. We test a culture‐derived model of ε_p37:2and find that the quantitative relationships calibrated in culture experiments can be used to predict ε_p37:2in sediment samples. In water‐column samples, the model substantially overestimates ε_p37:2, largely resulting from higher irradiance at the depth of sample collection than the integrated light conditions under which the sampled biomass was produced and vertically mixed to the collection depth. We argue that the theory underpinning the conventional diffusive alkenone carbon isotope fractionation model, including the “b” parameter, is not supported by field data and should not be used to reconstruct past CO₂changes. Future estimates of CO₂from ε_p37:2should use empirical or mechanistic models to quantitatively account for irradiance and cell size variations.