Transposable elements play a pivotal role in genome evolution and phenotypic variation in numerous eukaryotic species. Helitrons, a recently identified category of transposons, remain poorly understood in terms of epigenetic regulation and real-time mobilization in plants. Here our study reveals that reduced DNA methylation combined with heat stress promotes the mobilization of the Xuan–Feng Helitron family in wheat. Activation is marked by transcription, extrachromosomal circular DNA formation and novel somatic insertions. Genetic segregation and heterologous reconstitution establish Feng8 as the autonomous driver of the Xuan–Feng family mobilization. These findings represent a step forward in the study of active Helitrons and their potential biological functions as well as their role in genome dynamics and their potential use in crop breeding.