33Sustainable food production in the context of climate change necessitates diversification of 34 agriculture and a more efficient utilization of plant genetic resources. Fonio millet (Digitaria 35 exilis) is an orphan African cereal crop with a great potential for dryland agriculture. Here, we 36 established high-quality genomic resources to facilitate fonio improvement through molecular 37 breeding. These include a chromosome-scale reference assembly and deep re-sequencing of 183 38 cultivated and wild Digitaria accessions, enabling insights into genetic diversity, population 39 structure, and domestication. Fonio diversity is shaped by climatic, geographic, and ethnolinguistic 40 factors. Two genes associated with seed size and shattering showed signatures of selection. Most 41 known domestication genes from other cereal models however have not experienced strong 42 selection in fonio, providing direct targets to rapidly improve this crop for agriculture in hot and 43 dry environments. 44 45 agriculture 1-3 . The Food and Agriculture Organization of the United Nations (FAO) stated that arid 50 and semi-arid regions are the most vulnerable environments to increasing uncertainties in regional 51 and global food production 4 . In most countries of Africa and the Middle East, agricultural 52 productivity will decline in the near future 4 , because of climate change, land degradation, and 53 groundwater depletion 5 . Agricultural selection, from the early steps of domestication to modern-54 day crop breeding, has resulted in a marked decrease in agrobiodiversity 6,7 . Today, three cereal 55 4 crops alone, bread wheat (Triticum aestivum), maize (Zea mays), and rice (Oryza sativa) account 56 for more than half of the globally consumed calories 8 . 57Many of today's major cereal crops, including rice and maize, originated in relatively humid 58 tropical and sub-tropical regions 9,10 . Although plant breeding has adapted the major cereal crops 59 to a wide range of climates and cultivation practices, there is limited genetic diversity within these 60 few plant species for cultivation in the most extreme environments. On the other hand, crop wild 61 relatives and orphan crops are often adapted to extreme environments and their utility to unlock 62 marginal lands for agriculture has recently regained interest 2,6,[11][12][13][14] . Current technological advances 63 in genomics and genome editing provide an opportunity to rapidly domesticate wild relatives and 64 to improve orphan crops 15,16 . De novo domestication of wild species or rapid improvement of semi-65 domesticated crops can be achieved in less than a decade by targeting a few key genes 6 . 66White fonio (Digitaria exilis (Kippist) Stapf) (Fig. 1) is an indigenous African millet species with 67 a great potential for agriculture in marginal environments 17,18 . Fonio is cultivated under a large 68 range of environmental conditions, from a tropical monsoon climate in western Guinea to a hot, 69 arid desert climate (BWh) in the Sahel zone. Some extra-early matur...