DNA methylation erasure is required for mammalian primordial germ cell (PGC) reprogramming, including the erasure and appropriate re-establishment of genomic imprints. Until recently it was unclear what role passive (replication-coupled dilution) or active demethylation (through the TET family of enzymes) play in this reprogramming. We have shown that absence of Tet1 resulted in defective reprogramming of genomic imprints, although the mechanism remains poorly defined. Thus, the active process of demethylation in mammals requires TET enzymes. These enzymes iteratively oxidize 5-methylcytosine to generate 5-hyroxymethylcytosine (5hmC), 5-formylcytosine, and 5-carboxycytosine to facilitate active genome demethylation. Whether these bases are required to promote replication-coupled dilution or activate base excision repair during germline reprogramming also remains unresolved due to the lack of genetic models that decouple TET activities. We have generated two mouse lines expressing catalytically inactive TET1 (Tet1-HxD) and TET1 that stalls oxidation at 5hmC (Tet1-V). Tet1^-/-, Tet1^V/V, and Tet1^HxD/HxD  PGCs show failure in methylation erasure at imprinting control regions and promoters of meiosis associated genes, establishing the requirement for iterative oxidation of 5mC by TET1 for complete germline reprogramming at these regions. Full-length TET1^V and TET1^HxD rescue most hypermethylated regions of Tet1^-/- sperm, demonstrating the role of TET1 beyond its oxidative capability in patterning the sperm methylome. We further discovered a broader class of hypermethylated regions in sperm of Tet1 mutant mice that are excluded from de novo methylation during male germline development and depend on TET oxidation for reprogramming. This study underscores the link between TET1-mediated demethylation during reprogramming and methylome patterning in the germline.