DNA methylation enables recurrent endogenization of giant viruses in an animal relative DNA methylation (5mC) is a widespread mechanism for silencing genomic parasites in eukaryotes. While 5mC has complex roles in gene regulation beyond parasite control, it is most widely associated with transposable element (TE) silencing. In animals, 5mC shows widespread variability across lineages, ranging from gene regulation to loss of this base modification. This study shows that the protist Amoebidium appalachense, closely related to animals, features both transposon and gene body methylation, a pattern reminiscent of invertebrates and plants. Unexpectedly, large hypermethylated regions of the Amoebidium genome derive from viral insertions, including hundreds of endogenized giant viruses contributing 14% of the encoded genes, an extent never reported before in any eukaryotic genome. Using a combination of inhibitors and functional genomic assays, the study demonstrates that 5mC silences these giant virus insertions. Alternative Amoebidium isolates show polymorphic giant virus insertions, highlighting a dynamic process of infection, endogenization, and purging. The results indicate that 5mC is critical for the controlled coexistence of newly acquired viral DNA into eukaryotic genomes, making Amoebidium a unique model to understand the hybrid origins of eukaryotic genomes. The Amoebidium genome presents both gene body and TE methylation. The study found that Amoebidium appalachense has a high global methylation level of 40%, exclusively within the CG dinucleotide context, setting it apart from most invertebrates and fungi. The genome contains a large number of TEs, with approximately 50% of the genome composed of TEs, a level unmatched in any unicellular holozoan. The study also identified hundreds of giant virus insertions, including pandoraviruses, adintoviruses, and Plavaka giant repeats. These insertions are highly methylated and suggest that complete viral genome integrations are rare, or that gene loss occurs rapidly after insertion. The study also found that Amoebidium encodes a canonical KDM4 orthologue, which is involved in chromatin regulation. The endogenized KDM4-like enzymes only contain the enzymatic JmjC domain, which is involved in histone demethylation. The study suggests that these enzymes could be used by the virus to avoid silencing by the host chromatin. The results indicate that 5mC is instrumental for silencing and minimizing the consequence of viral DNA acquisition. DNA methylation removal is sufficient for viral transcriptional reactivation. The study tested the effect of cytidine-analogues on 5mC levels and found that 5-Azacytidine decreased global methylation levels,DNA methylation enables recurrent endogenization of giant viruses in an animal relative DNA methylation (5mC) is a widespread mechanism for silencing genomic parasites in eukaryotes. While 5mC has complex roles in gene regulation beyond parasite control, it is most widely associated with transposable element (TE) silencing. In animals, 5mC shows widespread variability across lineages, ranging from gene regulation to loss of this base modification. This study shows that the protist Amoebidium appalachense, closely related to animals, features both transposon and gene body methylation, a pattern reminiscent of invertebrates and plants. Unexpectedly, large hypermethylated regions of the Amoebidium genome derive from viral insertions, including hundreds of endogenized giant viruses contributing 14% of the encoded genes, an extent never reported before in any eukaryotic genome. Using a combination of inhibitors and functional genomic assays, the study demonstrates that 5mC silences these giant virus insertions. Alternative Amoebidium isolates show polymorphic giant virus insertions, highlighting a dynamic process of infection, endogenization, and purging. The results indicate that 5mC is critical for the controlled coexistence of newly acquired viral DNA into eukaryotic genomes, making Amoebidium a unique model to understand the hybrid origins of eukaryotic genomes. The Amoebidium genome presents both gene body and TE methylation. The study found that Amoebidium appalachense has a high global methylation level of 40%, exclusively within the CG dinucleotide context, setting it apart from most invertebrates and fungi. The genome contains a large number of TEs, with approximately 50% of the genome composed of TEs, a level unmatched in any unicellular holozoan. The study also identified hundreds of giant virus insertions, including pandoraviruses, adintoviruses, and Plavaka giant repeats. These insertions are highly methylated and suggest that complete viral genome integrations are rare, or that gene loss occurs rapidly after insertion. The study also found that Amoebidium encodes a canonical KDM4 orthologue, which is involved in chromatin regulation. The endogenized KDM4-like enzymes only contain the enzymatic JmjC domain, which is involved in histone demethylation. The study suggests that these enzymes could be used by the virus to avoid silencing by the host chromatin. The results indicate that 5mC is instrumental for silencing and minimizing the consequence of viral DNA acquisition. DNA methylation removal is sufficient for viral transcriptional reactivation. The study tested the effect of cytidine-analogues on 5mC levels and found that 5-Azacytidine decreased global methylation levels,