We have characterized the genetic and molecular origin of the reiterated reproductive meristem (RRM) somatic variant phenotype of grapevine cultivar Carignan. Here, we show that the extreme cluster proliferation and delayed anthesis observed in this somatic variant is caused by a single dominant mutation. Transcriptional profiling of Carignan and RRM plants during early stages of inflorescence development demonstrated the overexpression of a few regulatory genes, including VvTFL1A, a close TFL1 Arabidopsis homolog, in RRM inflorescences. Genetic and molecular analyses correlated the insertion of a class-II transposable element, Hatvine1-rrm, in the VvTFL1A promoter, with upregulation of the corresponding VvTFL1A allele in reproductive and vegetative organs of the shoot apex. These results suggest a role for this TFL1 grapevine homolog in the determination of inflorescence structure, with a critical effect on the size and branching pattern of grapevine fruit clusters. Our results demonstrate the existence of spontaneous cis-activation processes caused by class-II transposable elements in grapevine plants, and point to their possible role as a mechanism to generate somatic cell variation in perennial plants. This mechanism is expected to generate dominant phenotypes in chimeric sectors that can be readily exposed to natural selection.