Finger millet (Eleusine coracana Gaertn.), a nutritionally rich and drought-resilient C4 cereal, possesses exceptional grain storage longevity (up to 50 years). Here, we report a high-quality genome assembly of the allotetraploid cultivar C142, revealing extensive structural rearrangements between its two subgenomes (subA and subB), which are associated with asymmetric gene expression and subgenome dominance favoring subA. SubB diverged from its presumed progenitor E. indica approximately 6.8 million years ago, and two whole-genome duplication events shaped the current genome architecture, contributing to gene redundancy and adaptive potential. Notably, expansion of stress-related gene families, such as aldo-keto reductases, suggests a role in oxidative stress response and drought adaptation. Using genome-wide association studies (GWAS), we identify several candidate genes associated with key agronomic traits. Among them, EcMDHAR, encoding monodehydroascorbate reductase, plays a critical role in enhancing drought tolerance. Different EcMDHAR haplotypes exhibit distinct expression profiles, supporting their functional relevance in drought adaptation. This genomic resource not only advances our understanding of polyploid genome evolution in millets but also provides a foundation for genome-assisted improvement of drought resistance and nutritional quality in finger millet.