Anthracnose caused by Colletotrichum spp. is an economically important disease of many plants, including grain, vegetable, and fruit crops. Next-generation sequencing technologies have led to a dramatic growth in the size and availability of genomic data in public repositories. Beginning with genome sequencing projects of C. higginsianum and C. graminicola, many Colletotrichum spp. genomes have been sequenced due to their scientific and agricultural importance. Today, we can access more than a hundred genome assemblies of Colletotrichum spp. Utilizing those abundant genomic datasets would enable a better understanding of adaptation mechanisms of Colletotrichum spp. at the genomic level, which could help to control this important group of pathogens. In this review, we outline the development and application of genomic resources of Colletotrichum spp. with a focus on the benefits of genomic data-driven studies, including reverse-genetics, a range of comparative genomic analyses, species identification, taxonomy, and diagnosis, while describing the potential pitfalls of genome analysis. Further, we discuss future research directions that could allow a more comprehensive understanding of genomic diversity within the genus Colletotrichum.