Significance Human blood cell production is coordinated to ensure balanced levels of all lineages. The basis of this regulation remains poorly understood. Identification of genetic differences in human populations associated with blood cell measurements can shed light on such regulatory mechanisms. Here, we used whole-genome sequencing data to perform a genetic association study in a population-based biobank from Estonia. We identified a number of potential causal variants and underlying mechanisms. For example, we identified a regulatory element that is necessary for basophil production, which acts specifically during this process to regulate expression of the transcription factor CEBPA. We demonstrate how genome sequencing, genetic fine-mapping, and functional data can be integrated to gain important insight into blood cell production.