DNA methylation at the fifth position of cytosine (5mC) and at the sixth position of adenine (6 mA) plays an important role in the regulation of the gene expression and, in eukaryotes, is essential for normal development. For Ixodes ricinus, the most common European arthropod vector of human and animal pathogens, the DNA methylation profile and the role of DNA methylation in tick development are still under discussion. Our goal was to analyze the status of I. ricinus DNA methylation at different life stages and identify enzymes that produce this type of DNA modification. We found that 5mC and 6mA are present in I. ricinus genomic DNA at all life stages. In the transcriptome of I. ricinus, we identified the sequences of the putative IrDNMT1, IrDNMT3, and IrDAMT enzymes, and bioinformatic analysis and three-dimensional modeling predicted their DNA methylation activity. This confirms that I. ricinus possesses a complete DNA methylation toolkit. Our results suggest that DNA methylation is important for the physiology and transstadial development of ticks.