Epigenetic regulation involves changes in gene expression independent of DNA sequence variation that are inherited through cell division (Holliday, 2006). In addition to a fundamental role in cell differentiation, some epigenetic changes can also be transmitted transgenerationally through meiosis (Heard and Martienssen, 2014). Epigenetic alterations (“epimutations”) could thus contribute to heritable variation within populations and be subject to evolutionary processes such as natural selection and drift (Burggren, 2016). However, this suggestion is controversial, partly because unlike classical mutations involving DNA sequence changes, key parameters such as the rate at which epimutations arise and their persistence are unknown. Here, we perform the first genome-wide study of epimutations in a metazoan organism. We use experimental evolution to characterise the rate, spectrum and stability of epimutations driven by small silencing RNAs in the model nematode C. elegans . We show that epimutations arise spontaneously at a rate ∼25 times greater than DNA sequence changes and typically have short half-lives of 2-3 generations. Nevertheless, some epimutations last at least 10 generations. Epimutations thus may contribute to evolutionary processes over a short timescale but are unlikely to bring about long-term divergence without further DNA sequence changes.