Cold seeps are globally distributed chemosynthetic ecosystems that exert important influences on deep-sea carbon cycling, yet the functional diversity and spatial organization of their microbial communities remain largely unresolved. Here, we establish the Cold Seep Ecosystem Exploration Project (CoSEEP), a global collaborative effort that integrates systematic sampling across diverse seep microhabitats collected over a decade to generate a comprehensive metagenomic resource for methane-seep ecosystems. This resource uncovers extensive previously uncharacterized genetic diversity within seep microbiomes and reveals a substantial reservoir of hidden metabolic potential encoded in microbial sequence dark matter. By resolving microbial communities across fine spatial scales, we identify key environmental factors shaping microbial niche differentiation and uncover cryptic protein families associated with previously overlooked carbon transformation pathways, including potential contributions to methane metabolism. Functional and biotechnological exploration further demonstrates the value of this genomic resource for discovering novel microbial functions and genetic resources. Together, these findings advance our understanding of microbial regulation of deep-sea carbon cycling, provide a foundation for conserving vulnerable seep ecosystems, and expand opportunities for harnessing the unexplored genetic potential of deep-sea microbiomes.