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Summary: Actin depolymerizing factor (ADF) is a key modulator for dynamic organization of actin cytoskeleton. Interestingly, it was found that the ADF1 gene silencing delays flowering, but its mechanism remains unclear. In this study, ADF1 was used as a bait to screen its interacting proteins by the yeast two‐hybrid (Y2H) system. One of them, the REM16 transcription factor was identified. As one of the AP2/B3‐like transcriptional factor family members, the REM16 contains two B3 domains and its transcript levels kept increasing during the floral transition stage. Overexpression of REM16 accelerates flowering while silencing of REM16 delays flowering. Gene expression analysis indicated that the key flowering activation genes such as CONSTANS (CO), FLOWERING LOCUS T (FT), LEAFY (LFY) and SUPPRESSOR OF OVEREXPRESSION OF CONSTANS (SOC1) were upregulated in the REM16 overexpression lines, while the transcription of the flowering suppression gene FLOWERING LOCUS C (FLC) was decreased. In contrast, the REM16 gene silencing lines contained lower transcript levels of the CO, FT, LFY and SOC1 but higher transcript levels of the FLC compared with the wild‐type plants. It was proved that REM16 could directly bind to the promoter regions of SOC1 and FT by in vitro and in vivo assays. Genetic analysis supported that REM16 acts upstream of SOC1 and FT in flowering pathways. All these studies provided strong evidence demonstrating that REM16 promotes flowering by directly activating SOC1 and FT. Significance Statement: REM16 was isolated from the ADF1‐interacting protein screen by yeast two‐hybrid system. As a B3 domain transcription factor, REM16 can directly bind to the promoters of SOC1 and FT genes for promoting their expressions. Overexpression of REM16 promotes flowering, while suppression of REM16 delays flowering in Arabidopsis. Genetic analysis provided evidence to support that REM16 acts upstream of SOC1 and FT and plays a key role in flowering pathways. [ABSTRACT FROM AUTHOR]