Early vertebrate embryos must achieve totipotency and prepare for zygotic genome activation (ZGA). To understand this process, we determined the DNA methylation (DNAme) profiles of zebrafish gametes, embryos at different stages, and somatic muscle and compared them to gene activity and histone modifications. Sperm chromatin patterns are virtually identical to those at ZGA. Unexpectedly, the DNA of many oocyte genes important for germline functions (i.e., piwil1) or early development (i.e., hox genes) is methylated, but the loci are demethylated during zygotic cleavage stages to precisely the state observed in sperm, even in parthenogenetic embryos lacking a replicating paternal genome. Furthermore, this cohort constitutes the genes and loci that acquire DNAme during development (i.e., ZGA to muscle). Finally, DNA methyltransferase inhibition experiments suggest that DNAme silences particular gene and chromatin cohorts at ZGA, preventing their precocious expression. Thus, zebrafish achieve a totipotent chromatin state at ZGA through paternal genome competency and maternal genome DNAme reprogramming. Display omitted •Sperm chromatin patterns mirror the blastomere at zygotic genome activation (ZGA)•Maternal chromatin patterns are reprogrammed to the paternal/sperm state by ZGA•Maternal reprogrammed/demethylated genes are all later methylated in development•Promoter DNA methylation prevents precocious expression of particular genes at ZGA In the zebrafish zygote, the maternal genome undergoes considerable DNA methylation changes so that it conforms to the paternal pattern by the time zygotic genes are activated, a process that helps establish a totipotent zygotic genome.