The evolutionary ecology of prokaryotes within oceanic trenches remains largely unexplored. Here, we analyzed 19,194 medium-quality prokaryoti metagenomic assembled genomes (MAGs) from sediments of the Diamantina, Kermadec, Yap and Mariana trenches. Hadal zones hosted relatively ancient phylogenetic lineages across most prokaryotic phyla compared to non-hadal zones. A linear correlation between depth differences and the pairwise patristic distances was observed inter/intra trenches, indicating a depth-dependent evolutionary boundary. This pattern was further reflected by a clear vertical shift of genomic features, including carbon/nitrogen atoms per amino-acid-residue side chain (C/N-ARSC), pseudogene density and non-synonymous to synonymous mutation ratio (pN/pS). Close phylogenomic relationships for MAGs among different trenches suggested a rapidly and continuously exchange, which was very likely facilitated by deep-sea currents. Molecular dating of hadal Nitrososphaeria and Alphaproteobacteria revealed a divergence of respective 2.2 and 1.8 billion years ago, earlier than the emergence of contemporary trenches, emphasized the hadal zone sediments as a crucial ecological reservoir for prokaryotic evolution.