Flowering is controlled by a series of signals integrated to regulate gene expression and coordinate development. The flowering hormone FLOWERING LOCUS T (FT) positively regulates flowering while the highly homologous TERMINAL FLOWERING 1 (TFL1) negatively regulates flowering. FT is recruited to the promoter in a complex with FD, a transcription factor belonging to the bZIP family, and 14-3-3. This complex is called flowering activating complex (FAC). Here TFL1 is shown to form a complex with 14-3-3 proteins and FD that has striking similarity to the FAC. By probing the extended loop of TFL1 a small region was identified towards the N-terminus of the loop that is involved in mediating the interaction with 14-3-3. This TFL1–14-3-3 platform can interact with the C-terminus of FD, and moreover this interaction occurs between FD and 14-3-3 rather than directly between FD and TFL1 as had been previously speculated. Results indicate that the TFL1–14-3-3 complex, but not FT–14-3-3, can interact with the AP1 promoter from Arabidopsis and that FD is not required for this interaction. In addition, we have located a region of three residues near the C-terminal portion of the loop that when mutated can convert FT from an activator of flowering into a strong repressor of flowering in vivo. Overall, the results suggest that TFL1 can associate with DNA and recruit FD to specific regulatory sites via 14-3-3 proteins, while FT is recruited via FD to a different region within the AP1 promoter region. The data thus provide the basis for a mechanistic model for the antagonistic functions of FT and TFL1 in regulating flowering.