Peanut and soybean are legumes (Fabaceae) grown for their highly nutritious seeds and their ability to fix nitrogen in the soil. They are both tetraploids, with two sets of ten chromosomes (2n = 2x = 20 chromosomes) – soybean having undergone a whole genome duplication some 20 million years ago, and peanut approximately 10 thousand years ago. Peanut’s recent tetraploid origin, through a single hybridization event between two diploid progenitors, and the genetic bottleneck at the allotetraploid origin, have contributed to the narrow genetic diversity in this cultivated species. Using a set of 16 diverse peanut accessions, we evaluated and showed that subgenome exchanges accounted for > 10% of the observed allelic diversity among those accessions, showing that this genetic mechanism provides an explanation for the genetic diversity observed in peanut. We evaluated the ability to infer marker-trait associations using a subset of the USDA peanut core collection (the “mini-core”). This work paved the way and led to the genotyping of the entire USDA peanut core collection and the subsequent release of this data to the community. The ability for GWAS to identify marker-trait associations was limited by the close genetic similarity between accessions in the diversely sourced USDA peanut core and mini core collections, due to extensive population structure in the recently-derived allotetraploid species. On average, linkage disequilibrium decayed to a baseline of r2 = 0.2 at ~ 4,800 Kbp in peanut compared to ~238 Kbp, in the euchromatin, and 1,648 Kbp, in the heterochromatin, in soybean. Although such large LD blocks limit mapping resolution, it also implies that a fairly sparse marker coverage is sufficient to resolve trait architectures. We successfully mapped and identified variants explaining variation in fatty acid composition in peanut using ~14,000 markers. We showed that pleiotropic, additive, and epistatic effects of allelic variants contributed to the observed variation in fatty acid composition in the peanut core collection. This dissertation follows manuscripts that address the following three areas: 1) evaluating the USDA peanut mini core collection for genomic attributes that impact high-quality marker-trait associations, 2) genotyping and characterizing the USDA peanut core collection, and 3) mapping for the variability of fatty acid composition in peanut.