The germ cell lineage exhibits unique characteristics, which are essential towards generating totipotency. Among the distinctive events in this lineage is DNA demethylation and the erasure of parental imprints, which occur on embryonic day 11.5 (E11.5) after the primordial germ cells (PGCs) have entered into the developing gonads 12. Little is yet known about the mechanism involved, except that this appears to be an active process. Here we have examined the associated changes in the chromatin to gain further insights into this reprogramming event. We show that chromatin changes during this process occur in two-steps. The first changes observed in nascent PGCs at E8.5 establish a distinctive chromatin signature with some characteristics associated with pluripotency. Subsequently, at E11.5 when these PGCs are residing in the gonads, major changes occur in nuclear architecture with an extensive erasure of several histone modification marks along with exchange of histone variants. Furthermore, at this time, the histone chaperones, HIRA and NAP1, which are implicated in histone exchange, show accumulation in PGC nuclei undergoing reprogramming. We thus suggest that the mechanism of histone replacement is critical for these chromatin rearrangements to occur. The striking chromatin changes we show here are intimately linked with the process of genome-wide DNA demethylation. Based on the timing of the observed events, we propose, that if DNA demethylation entails DNA repair based mechanism, the evident histone replacement would rather than being a prerequisite, represent a repair-induced response event.