Transposable elements (TEs) are ubiquitous DNA sequences capable of self-propagating across genomes. To limit their mutagenic potential, TEs are typically controlled by epigenetic mechanisms, including DNA methylation in plants and mammals. Nonetheless, TEs eventually evade their epigenetic silencing and transpose. Using Arabidopsis thaliana, we recently reported that the mobilome of this species spans more than 150 TE families, and that the transposition rate in nature varies across ecotypes in association with genetic and environmental factors. Nonetheless, only a few Arabidopsis TEs have been observed to transpose experimentally so far, raising the question of what genetic and environmental factors control transposition. Here, we set out to measure the rate of heritable transposition using a comprehensive panel of genetically diverse Arabidopsis plants subjected to a range of environmental conditions. Overall, we detected significant heritable mobilization for at least 34 TE families, spanning both retrotransposons and DNA transposons. Importantly, we show that epigenetic perturbations are sufficient to trigger transposition bursts in a TE-specific manner, with the environment playing a secondary, modulatory role in TE mobilization. Unexpectedly, we found that some epigenetic mutants triggering extensive DNA hypomethylation, such as those affecting the chromomethylases CMT2 and CMT3, are dispensable for controlling transposition. To investigate the molecular mechanism underlying TE activity, we studied the developmental window where heritable transcription takes place, by collecting seeds derived from flowers from the same or different inflorescence, and from different stems. Overall, the segregation pattern of new insertions reveals that distinct TEs transpose at different reproductive stages, and that the environment shapes the developmental window in which transposition is occurring. Our work provides a first genetic and environmental (GxE) interaction map of transposition and sets the basis for uncovering the molecular mechanisms controlling the developmental specificity of TE reactivation.