Legume crops, belonging to the Fabaceae family, are of immense importance for sustaining global food security. Many legumes are profitable crops for smallholder farmers due to their unique ability to fix atmospheric nitrogen and their intrinsic ability to thrive on marginal land with minimum inputs and low cultivation costs. Recent progress in genomics shows promise for future genetic gains in major grain legumes. Still it remains limited in minor legumes/underutilized legumes, including adzuki bean, cluster bean, horse gram, lathyrus, red clover, urd bean, and winged bean. In the last decade, unprecedented progress in completing genome assemblies of various legume crops and resequencing efforts of large germplasm collections has helped to identify the underlying gene(s) for various traits of breeding importance for enhancing genetic gain and contributing to developing climate-resilient cultivars. This review discusses the progress of genomic resource development, including genome-wide molecular markers, key breakthroughs in genome sequencing, genetic linkage maps, and trait mapping for facilitating yield improvement in underutilized legumes. We focus on 1) the progress in genomic-assisted breeding, 2) the role of whole-genome resequencing, pangenomes for underpinning the novel genomic variants underlying trait gene(s), 3) how adaptive traits of wild underutilized legumes could be harnessed to develop climate-resilient cultivars, 4) the progress and status of functional genomics resources, deciphering the underlying trait candidate genes with putative function in underutilized legumes 5) and prospects of novel breeding technologies, such as speed breeding, genomic selection, and genome editing. We conclude the review by discussing the scope for genomic resources developed in underutilized legumes to enhance their production and play a critical role in achieving the “zero hunger” sustainable development goal by 2030 set by the United Nations.