The transcription factor CONSTANS (CO) integrates day‐length information to induce the expression of florigen FLOWERING LOCUS T (FT) in Arabidopsis. We recently reported that the C‐terminal CCT domain of CO forms a complex with NUCLEAR FACTOR‐YB/YC to recognize multiple cis‐elements in the FT promoter, and the N‐terminal tandem B‐box domains form a homomultimeric assembly. However, the mechanism and biological function of CO multimerization remained unclear. Here, we report that CO takes on a head‐to‐tail oligomeric configuration via its B‐boxes to mediate FT activation in long days. The crystal structure of B‐boxesCO reveals a closely connected tandem B‐box fold forming a continuous head‐to‐tail assembly through unique CDHH zinc fingers. Mutating the key residues involved in CO oligomerization resulted in a non‐functional CO, as evidenced by the inability to rescue co mutants. By contrast, a transgene encoding a human p53‐derived tetrameric peptide in place of the B‐boxesCO rescued co mutant, emphasizing the essential role of B‐boxesCO‐mediated oligomerization. Furthermore, we found that the four TGTG‐bearing cis‐elements in FT proximal promoter are required for FT activation in long days. Our results suggest that CO forms a multimer to bind to the four TGTG motifs in the FT promoter to mediate FT activation. Examination of the crystal structure of Nterminal tandem B‐box domains of CONSTANS (CO), the key player in photoperiod flowering pathway, reveals that B‐Boxes of CO form a head‐to‐tail type linear oligomer, which mediates the multimeric assembly of CO to enhance the accurate targeting of CO to FLOWERING LOCUS T.