This study demonstrates the generation of primordial germ cell-like cells (PGCLCs) in mice, which have robust capacity for spermatogenesis. PGCLCs were generated from embryonic stem cells (ESCs) and induced pluripotent stem cells (iPSCs) through epiblast-like cells (EpiLCs), a cellular state similar to pregastrulating epiblasts but distinct from epiblast stem cells (EpiSCs). The induction of EpiLCs from ESCs/iPSCs is a progressive process, and EpiLCs competent for the PGC fate are transient. The global transcription profiles, epigenetic reprogramming, and cellular dynamics during PGCLC induction from EpiLCs closely resemble those associated with PGC specification from the epiblasts. Integrin-β3 and SSEA1 were identified as markers for isolating PGCLCs with spermatogenic capacity from undifferentiated cells. These findings provide a paradigm for the first step of in vitro gametogenesis.This study demonstrates the generation of primordial germ cell-like cells (PGCLCs) in mice, which have robust capacity for spermatogenesis. PGCLCs were generated from embryonic stem cells (ESCs) and induced pluripotent stem cells (iPSCs) through epiblast-like cells (EpiLCs), a cellular state similar to pregastrulating epiblasts but distinct from epiblast stem cells (EpiSCs). The induction of EpiLCs from ESCs/iPSCs is a progressive process, and EpiLCs competent for the PGC fate are transient. The global transcription profiles, epigenetic reprogramming, and cellular dynamics during PGCLC induction from EpiLCs closely resemble those associated with PGC specification from the epiblasts. Integrin-β3 and SSEA1 were identified as markers for isolating PGCLCs with spermatogenic capacity from undifferentiated cells. These findings provide a paradigm for the first step of in vitro gametogenesis.