The repressive capacity of cytosine DNA methylation is mediated by recruitment of silencing complexes by methyl-CpG binding domain (MBD) proteins. Unexpectedly, we discovered that a family of arthropod Copia retrotransposons have incorporated a host-derived MBD domain. We functionally demonstrate how retrotransposon encoded MBDs preferentially bind to CpG-dense methylated regions, which correspond to transposable element regions of the host genome, in the myriapod Strigamia maritima. Consistently, young MBD-encoding Copia retrotransposons (CopiaMBD) accumulate in regions with higher CpG-densities than other LTR-retrotransposons also present in the genome. This would suggest that retrotransposons use MBDs to integrate into heterochromatic regions in Strigamia, avoiding potentially harmful insertions into host genes. In contrast, CopiaMBD insertions in the spider Stegodyphus dumicola genome disproportionately accumulate in methylated gene bodies when compared to other spider LTR-retrotransposons. Given that transposons are not actively targeted by DNA methylation in the spider genome, this distribution bias would also support a role for MBDs in the integration process. Together, these data demonstrate that retrotransposons can co-opt host-derived epigenome readers, potentially harnessing the host epigenome landscape to advantageously tune the retrotransposition process. Overall design: Profiling of cytosine methylation of Strigamia maritima. DAP-seq and ampDAP-seq of retrotransposon encoded MBDs on Strigamia maritima genomic DNA.