FLOWERING LOCUS T (FT) regulates the floral transition in many plant species by integrating environmental seasonal signals and internal cues. Here we show that two interdependent regulatory regions are necessary and sufficient to convey photoperiod responsiveness to FT. While a minimal distance between the regulatory regions is required to fully suppress FT expression under short days, increased distance reduces promoter response to long days. Natural variation at FT creating promoter length differences is widespread, correlates with longitudinal and latitudinal clines and affects a promoter region physically interacting with both photoperiod control regions. Three major FT promoter variants correlate with differences in FT allele usage in F1 hybrids. We propose that FT variation in cis could be adaptive by conferring differences in FT transcriptional control ultimately translating to increased fitness.