The study of genetics involves the exploration of hereditary traits and their transmission across generations through the conveyance of genetic information. On a parallel track, epigenetic research investigates modifications that modulate gene expression without altering the DNA sequence itself. Transposable elements (TEs), which are repetitive DNA segments, exhibit rigorous control by epigenetic mechanisms due to their propensity to trigger diverse genetic alterations upon activation. TEs play a dynamic role akin to a balancing act, bridging the realms of genetics, epigenetics, and environment. Throughout their life cycle, distinct classes of TEs exhibit varying molecular mechanisms that can lead to the generation of extrachromosomal circular DNA (eccDNA). These eccDNAs can constitute an integral component of a TE's replication process. Consequently, the emergence of eccDNA can often be attributed to TE activation. The rapid advancements in high-throughput sequencing technologies and computational pipelines have facilitated a comprehensive exploration of plant eccDNA landscapes. Recent discoveries highlight that various genomic regions, such as telomeres, centromere satellites, and even genic domains can contribute to the eccDNA pool. While progress has been made in identifying genomic regions producing eccDNA, the precise cellular functions of these elements remain elusive in plants. In his study, we present a comprehensive study of eccDNAs in wheat. First, we studied the regions of the genome that can contribute to eccDNA accumulation and then investigated if external stimuli can influence eccDNA quality and quantity. Our findings revealed that in wheat, eccDNAs largely originate from regions including plastid sequences, ribosomal DNA, and truncated TEs. Though their composition remained stable under single stress treatment in wheat, combining epigenetic stress with heat stress led to the emergence of full-length eccDNAs derived from a non-autonomous Helitron, suggesting we for the first time, observed an active TE in wheat. This finding prompted us to carry out a comprehensive global analysis of Helitrons with a particular focus on the family we found to be mobilizable in wheat. This family consists of 85 members, of which merely six were classified as autonomous copies as they potentially encoded full-length transposases. Remarkably, these autonomous Helitrons exhibited copy number variations across different wheat cultivars, suggesting a recent mobilization activity for this TE. Notably only a subset of cultivars showed a transcriptional response to our treatment. We found that transcriptional activation co-incited with reduced DNA methylation levels within the genomic Helitron sequence, particularly at an identified heat shock factor binding site. This further supports the notion that this TE family is restricted by DNA methylation. A inspection of the transposases encoded by the autonomous copies present in the wheat genome led to the identification of key distinctive domains suggesting that they contain all necessary functional domains required for Helitron mobility. Finally, we evaluated whether our treatment could lead to phenotypic diversity suitable for wheat breeding.