DNA methylation is highly dynamic during mammalian embryogenesis. It is widely accepted that the paternal genome is actively depleted of 5-methylcytosine at fertilization, followed by passive loss that reaches a minimum at the blastocyst stage. However, this model is based on limited data, and no base-resolution maps exist to support and refine it. This study generated genome-scale DNA methylation maps in mouse gametes and through post-implantation embryogenesis. The oocyte already exhibits global hypomethylation, most prominently at specific families of long interspersed element-1 and long terminal repeat retro-elements. The oocyte contributes a unique set of differentially methylated regions (DMRs), including many CpG island promoter regions, which are maintained in the early embryo but are lost upon specification and absent from somatic cells. In contrast, sperm-contributed DMRs are largely intergenic and resolve to hypermethylation after the blastocyst stage. Our data provide a complete genome-scale, base-resolution timeline of DNA methylation in the pre-specified embryo, when this epigenetic modification is most dynamic, before returning to the canonical somatic pattern. The study reveals that the oocyte defines the early methylation landscape, with significant changes in methylation levels occurring during two developmental transitions: between sperm and the zygote and between the inner cell mass (ICM) and the post-implantation embryo. The oocyte contributes DMRs that are maintained in the early embryo but are lost upon specification, while sperm-contributed DMRs are largely intergenic and resolve to hypermethylation after the blastocyst stage. The study also shows that methylation levels in the early embryo do not resemble somatic patterns, with the oocyte methylation levels more closely resembling those of early embryonic time points than the levels in sperm, post-implantation embryos, or adult tissues. The study provides a comprehensive understanding of DNA methylation dynamics during early mammalian development, highlighting the unique regulatory phase of DNA methylation in the early mammalian embryo.DNA methylation is highly dynamic during mammalian embryogenesis. It is widely accepted that the paternal genome is actively depleted of 5-methylcytosine at fertilization, followed by passive loss that reaches a minimum at the blastocyst stage. However, this model is based on limited data, and no base-resolution maps exist to support and refine it. This study generated genome-scale DNA methylation maps in mouse gametes and through post-implantation embryogenesis. The oocyte already exhibits global hypomethylation, most prominently at specific families of long interspersed element-1 and long terminal repeat retro-elements. The oocyte contributes a unique set of differentially methylated regions (DMRs), including many CpG island promoter regions, which are maintained in the early embryo but are lost upon specification and absent from somatic cells. In contrast, sperm-contributed DMRs are largely intergenic and resolve to hypermethylation after the blastocyst stage. Our data provide a complete genome-scale, base-resolution timeline of DNA methylation in the pre-specified embryo, when this epigenetic modification is most dynamic, before returning to the canonical somatic pattern. The study reveals that the oocyte defines the early methylation landscape, with significant changes in methylation levels occurring during two developmental transitions: between sperm and the zygote and between the inner cell mass (ICM) and the post-implantation embryo. The oocyte contributes DMRs that are maintained in the early embryo but are lost upon specification, while sperm-contributed DMRs are largely intergenic and resolve to hypermethylation after the blastocyst stage. The study also shows that methylation levels in the early embryo do not resemble somatic patterns, with the oocyte methylation levels more closely resembling those of early embryonic time points than the levels in sperm, post-implantation embryos, or adult tissues. The study provides a comprehensive understanding of DNA methylation dynamics during early mammalian development, highlighting the unique regulatory phase of DNA methylation in the early mammalian embryo.