Soil harbors a vast expanse of unidentified microbes, termed as microbial dark matter, presenting an untapped reservoir of microbial biodiversity and genetic resources, but has yet to be fully explored. In this study, we conducted the first large-scale excavation of soil microbial dark matter by reconstructing 40,039 metagenome-assembled genome bins (the SMAG catalog) from 3,304 soil metagenomes. We identified 16,530 of 21,077 species-level genome bins (SGBs) as unknown SGBs (uSGBs), which greatly expand archaeal and bacterial diversity across the tree of life. We also illustrate the pivotal role of uSGBs in augmenting soil microbiome's functional landscape and intra-species genome diversity, providing large proportions of the 43,169 biosynthetic gene clusters and 8,545 CRISPR-Cas genes. Additionally, we determined that uSGBs contributed 84.6% of novel viral-host associations identified from the SMAG catalog. Our results propose the SMAG catalog, a novel and expansive genomic resource that brings the soil microbial biodiversity and novel genetic resources to light.