Advances in second/third-generation sequencing and computational innovations revolutionized our understanding of the genomic structure of Y-chromosomes and their unique phylogenetic features. However, the construction of population-specific high-resolution Y-chromosome panels and databases in anthropological and forensic translational applications is limited due to the unavailability of the population-scale genomic database. We developed the highest-resolution Y-targeted sequencing panel based on the screened time-stamped core phylogenetic informative mutations from high-coverage sequences in the YanHuang cohort to explore ethnolinguistically diverse Chinese people's fine-scale paternal evolutionary history. The evaluated sequencing performance of the 2999-core SNP variant calling observed in this East-Asian-specific Y-chromosomal panel was robust and reliable. The YHSeqY3000 panel was designed to capture the genetic diversity of Chinese 3500-year-ago paternal lineages and identified 408 terminal lineages in 2097 individuals from 41 genetically and geographically different populations. We identified fine-scale paternal substructure correlated with ancient population migrations and expansions and reported new evidence of the extensive gene flow events between minority ethnic groups and Han Chinese people based on the integrative Chinese paternal genomic diversity database (CPGDD). This work effectively integrated the Y-chromosome-related basis science and translational utilization, underscoring the necessity and importance of comprehensive characterization of Y-chromosome genomic diversity based on the dense sampling strategies in the second phase of population-specific medical or anthropological cohorts.