The fidelity of the early embryonic program is underlined by tight regulation of the chromatin. Yet, how the chromatin is organized to prohibit the reversal of the developmental program remains unclear. Specifically, the totipotency-to-pluripotency transition marks one of the most dramatic events to the chromatin, and yet, the nature of histone alterations underlying this process is incompletely characterized. Here, we show that linker histone H1 is post-translationally modulated by SUMO2/3, which facilitates its fixation onto ultra-condensed heterochromatin in embryonic stem cells (ESCs). Upon SUMOylation depletion, the chromatin becomes de-compacted and H1 is evicted, leading to totipotency reactivation. Furthermore, we show that H1 and SUMO2/3 jointly mediate the repression of totipotent elements. Lastly, we demonstrate that preventing SUMOylation on H1 abrogates its ability to repress the totipotency program in ESCs. Collectively, our findings unravel a critical role for SUMOylation of H1 in facilitating chromatin repression and desolation of the totipotent identity. [Display omitted] • Linker histone H1 is post-translationally SUMOylated in ESCs • SUMOylation of linker histone H1 drives its fixation onto condensed heterochromatin • Loss of SUMOylated H1 is associated with chromatin decompaction in ESCs • SUMOylation of H1 represses the reactivation of the totipotency program in ESCs Sheban et al. demonstrate that linker histone H1 is modified by SUMO to modulate the chromatin landscape and repress the totipotency program in ESCs. This process, in turn, ensures proper determination of early embryonic cell fate. [ABSTRACT FROM AUTHOR]