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The human leukocyte antigen (HLA) locus plays a critical role in complex traits spanning autoimmune and infectious diseases, transplantation, and cancer. While coding variation in genes has been extensively documented, regulatory genetic variation modulating expression levels has not been comprehensively investigated. Here, we mapped expression quantitative trait loci (eQTLs) for classical genes across 1,073 individuals and 1,131,414 single cells from three tissues, using personalized reference genomes to mitigate technical confounding. We identified cell-type-specific -eQTLs for every classical gene. Modeling eQTLs at single-cell resolution revealed that many eQTL effects are dynamic across cell states even within a cell type. genes exhibit particularly cell-state-dependent effects within myeloid, B, and T cells. Dynamic regulation may underlie important interindividual variability in immune responses.