This study investigates the mechanism by which transcription termination influences the local chromatin environment in *Arabidopsis*. The authors identify an *APRF1* (a homolog of yeast Swd2 and human WDR82)-containing CPF-like phosphatase module that interacts with an H3K4me1 demethylase, linking RNA processing to chromatin modification. APRF1, in this module, works with TOPP4 (Glc7/PP1) and LD (Ref2/PNUTS) to regulate transcription termination and subsequent chromatin remodeling. Loss of *APRF1* leads to transcriptional readthrough and hyperphosphorylation of RNA Pol II, altering the local chromatin environment at the *FLOWERING LOCUS C (FLC)* locus. This chromatin environment reinforces proximal termination, providing a molecular feedback mechanism to maintain a low transcriptional state. The study also highlights the functional divergence of *APRF1* and S2LB in Arabidopsis, with *APRF1* acting in the 3' processing machinery and S2LB interacting with COMPASS to activate *FLC*. The findings suggest that the APRF1-LD-TOPP4 module forms a plant equivalent of the yeast and human CPF phosphatase modules, linking transcription termination to histone demethylation and chromatin silencing.This study investigates the mechanism by which transcription termination influences the local chromatin environment in *Arabidopsis*. The authors identify an *APRF1* (a homolog of yeast Swd2 and human WDR82)-containing CPF-like phosphatase module that interacts with an H3K4me1 demethylase, linking RNA processing to chromatin modification. APRF1, in this module, works with TOPP4 (Glc7/PP1) and LD (Ref2/PNUTS) to regulate transcription termination and subsequent chromatin remodeling. Loss of *APRF1* leads to transcriptional readthrough and hyperphosphorylation of RNA Pol II, altering the local chromatin environment at the *FLOWERING LOCUS C (FLC)* locus. This chromatin environment reinforces proximal termination, providing a molecular feedback mechanism to maintain a low transcriptional state. The study also highlights the functional divergence of *APRF1* and S2LB in Arabidopsis, with *APRF1* acting in the 3' processing machinery and S2LB interacting with COMPASS to activate *FLC*. The findings suggest that the APRF1-LD-TOPP4 module forms a plant equivalent of the yeast and human CPF phosphatase modules, linking transcription termination to histone demethylation and chromatin silencing.