TERMINAL FLOWER1 (TFL1) is a key regulator of Arabidopsis plant architecture, which responses to developmental and environmental signals to control flowering time and the fate of shoot meristems. TFL1 has a dynamic pattern of expression, being found in all shoot meristems, but not in floral meristems, with its level and distribution changing throughout development. Using a variety of complementary experimental approaches (phylogenetic shadowing, T-DNA lines, complementation analysis and promoter::GUS fusions), we have performed an intensive analysis to elucidate the functional structure of the TFL1 promoter. Our study reveals that TFL1 expression is based on distinct cis-regulatory regions, the most important ones, which direct expression to different domains of the shoot apex, are located 3' of the coding sequence. Our results further indicate that TFL1 expression in the main vs lateral inflorescence meristems is controlled through distinct cis-regulatory regions, suggesting that different signals control expression in these meristem types. Moreover, we identified a cis-regulatory region necessary for TFL1 expression in the vegetative shoot, that is required for a wild-type flowering time, supporting the model that TFL1 expression in the vegetative meristem controls flowering time. Our study provides a model for the functional organization of TFL1 cis-regulatory regions, contributing to our understanding of how developmental pathways are integrated at the genomic level of a key regulator to control plant architecture.