Winter-annual accessions of Arabidopsis thaliana require either exposure to cold stress or vernalization to initiate flowering via FRIGIDA (FRI). FRI acts as a scaffold protein to recruit several chromatin modifiers that epigenetically modify flowering genes. Here, we report that proteasome-mediated FRI degradation regulates flowering during vernalization in Arabidopsis. Our genetic and biochemical experiments demonstrate that FRI directly interacts with the BTB (Bric-a-Brac/Tramtrack/Broad Complex) proteins LIGHT-RESPONSE BTB1 (LRB1) and LRB2 as well as the CULLIN3A (CUL3A) ubiquitin-E3 ligase in vitro and in vivo, leading to proteasomal degradation of FRI during vernalization. The degradation of FRI is accompanied by an increase in the levels of the long noncoding RNA ColdAIR, which reduces the level of histone H3Lys4 trimethylation (H3K4me3) in FLOWERING LOCUS C chromatin to promote flowering. Furthermore, we found that the cold-induced WRKY34 transcription factor binds to the W-box in the promoter region of CUL3A to modulate CUL3A expression. Deficiency of WRKY34 suppressed CUL3A transcription to enhance FRI protein stability and led to late flowering after vernalization. Conversely, overexpression of WRK34 promoted FRI degradation and early flowering through inducing CUL3A accumulation. Together, these data suggest that WRKY34-induced and CUL3A-dependent proteolysis of FRI modulate flowering in response to vernalization.