In mammals, one of the two X chromosomes is inactivated in females to enable dosage compensation for X-linked gene products. In mice, the X chromosome of paternal origin (Xp) is silenced during early embryogenesis due to imprinted expression of the regulatory RNA, Xist (X-inactive-specific-transcript). This imprinted form of X inactivation is reversed in the inner cell mass (ICM) of the blastocyst and random X inactivation subsequently occurs in the epiblast. However, its ontogeny and mechanism in primates, including humans, remain unknown. Here, we delineate a distinct mechanism for X-chromosome inactivation (XCI) in key cell lineages in cynomolgus monkeys, a model for human development. With a common mechanism, while trophectoderm/cytotrophoblasts acquire XCI around implantation, amnion/epiblast/hypoblast exhibit a protracted intermediate state, attaining XCI by a week after implantation. Conversely, primordial germ cells (PGCs) undergo X-chromosome reactivation by faithfully reverting the XCI pathway early during their development. Crucially, males achieve X-chromosome up-regulation (XCU) progressively, whereas females show XCU interwoven with XCI, both establishing the X: autosome dosage compensation by one week after implantation. Our findings create an essential paradigm for the X-chromosome dosage compensation mechanism in primates.