The cultivated peanut (Arachis hypogaea), a leading food and oilseed crop in tropical and subtropical regions, contains multiple seed storage proteins identified as allergens that affect more than 0.8% of children and 0.6% of US adults. We sequenced ~ 600 kb from cultivated peanut and ~ 150 kb from wild species (A genome) to gain insights into genome organization and evolution of Arah1, Arah2 and Arah3 allergen genes. To assign polarity to differences between homoeologous regions in peanut, we used as outgroups the single orthologous regions in Medicago and Lotus, which diverged from peanut approximately 50 mya and have not undergone a subsequent polyploidy. We also compared these regions with orthologs in soybean, grape, tomato, poplar and Arabidopsis, to help clarify the timing of evolutionary events. The peanut allergen genes are interspersed with low-copy genes and transposable elements. Phylogenetic analyses revealed lineage-specific expansion and loss of low-copy genes between species and homoeologues. We infer that two rounds of segmental duplication and tandem duplications led to the establishment of the AraH3 gene family. Phylogenetic analysis and genomic organization studies provide new insights into evolution of major peanut allergen genes.