Persistence is a key characteristic of memory that relies on systems consolidation, a process classically defined as the gradual transfer of information from the hippocampus to the cortex for long-term memory storage. However, the underlying molecular mechanisms are unknown. DNA methylation can act as a long-term regulatory signal, therefore being a prime candidate to regulate memory duration and stabilisation within engrams– the physical substrate of a memory.Using contextual fear conditioning (CFC) and engram tagging tools in mice, we showed that reactivation of cortical engrams reflects systems consolidation. We found higher engagement of cortical engrams selectively in persistent fear memory. To address whether DNA methylation underlies persistent memory storage, we overexpressed a DNA Methyltransferase (Dnmt3a2) in the hippocampus of mice during CFC. Strikingly, we found a conversion of short-lasting into persistent memory. Moreover, we found an improved reactivation of cortical engrams and increased fear generalisation, mimicking the engram dynamics and behavioural trait of remote memory, respectively. Knockdown of hippocampal Dnmt3a2 reduced cortical engram reactivation and memory duration. Using chemogenetic inhibition of the cortical engram, we proved that the memory trace resides in the cortex. These findings demonstrate that DNA methylation processes facilitate the transfer of information from the hippocampus to the cortex for long-term storage.To gain mechanistic insight, we uncovered, using RNA-Sequencing, Dnmt3a2 target genes that may underlie memory persistence.In summary, we found that DNA methylation in dorsal hippocampus converts a short-lasting into a persistent memory by the facilitation of systems consolidation and associated stabilisation of cortical engrams.