Transposable elements (TEs) are responsible for rapid genome remodelling by the creation of new regulatory gene networks and chromosome restructuring. TEs are often regulated by the host through epigenetic systems, but environmental changes can lead to physiological and, therefore, epigenetic stress, which disrupt the tight control of TEs. The resulting TE mobilization drives genome restructuring that may sometimes provide the host with an innovative genetic escape route. We suggest that macroevolution and speciation might therefore originate when the host relaxes its epigenetic control of TEs. To understand the impact of TEs and their importance in host genome evolution, it is essential to study TE epigenetic variation in natural populations. We propose to focus on recent data that demonstrate the correlation between changes in the epigenetic control of TEs in species/populations and genome evolution.