SummaryMADS‐box genes encode a family of transcription factors that regulate diverse developmental programs in plants. The present work shows the regulation of flowering time by AGL6 through control of the transcription of both a subset of the FLOWERING LOCUS C (FLC) family genes and FT, two key regulators of flowering time. The agl6‐1D mutant, in which AGL6 was activated by the 35S enhancer, showed an early flowering phenotype under both LD and SD conditions. Its early flowering was additively accelerated by CONSTANS (CO) overexpression. The agl6‐1D mutation strongly suppressed the late flowering of fve‐4 and fca‐9 mutants. Endogenous AGL6 transcript accumulation was photoperiod‐independent and the AGL6:GFP protein was preferentially localized in the nucleus. In agl6‐1D plants, the expression of FLC, MADS AFFECTING FLOWERING (MAF) 4, and MAF5 was downregulated. Interestingly, late flowering of a functional FRIGIDA (FRI) FLC allele was dramatically suppressed by the agl6‐1D mutation. AGL6 activation in the flc‐3 background further enhanced FT expression, suggesting that AGL6 also regulates FT expression independently of FLC mRNA level. A near RNA‐null ft‐10 mutation completely suppressed early flowering of the agl6‐1D plants, suggesting that FT is a major downstream output of AGL6. Transgenic plants overexpressing an artificial microRNA targeting AGL6 showed a late‐flowering phenotype. In these plants, FT expression was downregulated, whereas FLC expression was upregulated. The present results suggest that AGL6 acts as a floral promoter with a dual role, the inhibition of the transcription of the FLC/MAF genes and the promotion of FT expression in Arabidopsis.