Anthracnose, caused by hemibiotrophic Colletotrichum spp., is a destructive disease of legumes and many other crops worldwide. Colletotrichum spp. constitute one of the top 10 phytopathogenic fungi, infecting ∼3,000 plant species, attacking food and forage legume crops at all growth stages; including seed, seedlings, young, and mature plants; with consequent significant yield reductions. Presently, cultural practices and substantial use of synthetic fungicides are the most prevalent approaches for anthracnose management. In addition, there has been a strong focus toward developing advanced breeding lines and cultivars with improved anthracnose resistance. This has involved traditional breeding resulting in a wide range of anthracnose resistance resources being identified, particularly using advanced techniques within the common bean, soybean, lentil, mungbean, blackgram, and lupins. For instance, quantitative trait loci (QTLs) for resistance have been identified, enabling marker-assisted resistance breeding. More recently, molecular approaches; including genomics, transcriptomics, proteomics, and metabolomics; have been utilized to understand the pathogenesis and defense mechanisms involved in the Colletotrichum-legume interaction. Genetic manipulation through omics offers scope to better protect legumes from anthracnose by improving the efficiency of breeding programs. This review focuses on key pathogens (viz., C. truncatum, C. lentis, C. lupini, and C. lindemuthianum) causing anthracnose in legumes, their biology, and epidemiology, the disease management levers embracing progress with host resistance, genetic and breeding approaches, and highlights critical knowledge gaps in conventional and molecular breeding programs. We conclude that the ongoing progress toward developing breeding lines/cultivars/donors with improved resistance in legume plant responses against anthracnose using omics approaches offers novel insights into legume-anthracnose pathogen interactions and ensures more sustainable and effective disease management strategies for the future.