Covalent PARylation of DNA base excision repair (BER) proteins regulates DNA demethylation. PARP1 and PARP2, ATP-ribosyltransferases, contribute to DNA base excision repair and DNA demethylation. Recent proteomic analyses identified BER proteins as covalently poly-ADP-ribosylated by PARPs. This study shows that PARP1 senses AP-sites and SSBs generated during TET-TDG mediated active DNA demethylation and covalently attaches PAR to BER proteins. Covalent PARylation dissociates BER proteins from DNA, accelerating repair. Inhibition of PARylation in mESC reduced DNA demethylation and repair of random DNA damage. PARylation reduces DNA affinity of BER proteins, facilitating their dissociation from DNA after repair, allowing them to re-engage in new cycles of BER, thus increasing DNA demethylation efficiency. PARylation modulates protein-DNA interactions in BER to promote TDG-dependent active DNA demethylation in ESCs. PARylation of BER proteins, including TDG, XRCC1, POLβ, APE1, and LIG3, is triggered by AP-sites. PARylation reduces DNA affinity of BER proteins, promoting their dissociation from DNA. PARylation of BER proteins is essential for efficient turnover of fC and caC by TDG-BER. PARylation of BER proteins is regulated by PARP and PARG activities. PARylation of BER proteins is important for DNA repair and chromatin association. PARylation of BER proteins interferes with DNA binding. PARylation of XRCC1 reduces DNA damage association in cells. PARylation promotes repair of DNA demethylation- and DNA damage-associated SSBs. PARylation is necessary for recruitment of DNA damage response factors to sites of spontaneous DNA damage. PARylation is required for turnover of engaged BER/SSBR. PARylation has a dual role in promoting enzymatic turnover in active DNA demethylation and in SSBR. PARylation is an integral part of targeted BER in the context of active DNA demethylation, where it regulates the coordinated action of TDG and the BER proteins. PARylation is a general feature of BER, as several DNA glycosylases are also PARylated following exposure to oxidative stress. PARylation controlled assembly and disassembly of protein complexes provide a mechanistic framework to explain the coordination and dynamics of complex multi-enzyme transactions involved in DNA repair and the maintenance of genomic function.Covalent PARylation of DNA base excision repair (BER) proteins regulates DNA demethylation. PARP1 and PARP2, ATP-ribosyltransferases, contribute to DNA base excision repair and DNA demethylation. Recent proteomic analyses identified BER proteins as covalently poly-ADP-ribosylated by PARPs. This study shows that PARP1 senses AP-sites and SSBs generated during TET-TDG mediated active DNA demethylation and covalently attaches PAR to BER proteins. Covalent PARylation dissociates BER proteins from DNA, accelerating repair. Inhibition of PARylation in mESC reduced DNA demethylation and repair of random DNA damage. PARylation reduces DNA affinity of BER proteins, facilitating their dissociation from DNA after repair, allowing them to re-engage in new cycles of BER, thus increasing DNA demethylation efficiency. PARylation modulates protein-DNA interactions in BER to promote TDG-dependent active DNA demethylation in ESCs. PARylation of BER proteins, including TDG, XRCC1, POLβ, APE1, and LIG3, is triggered by AP-sites. PARylation reduces DNA affinity of BER proteins, promoting their dissociation from DNA. PARylation of BER proteins is essential for efficient turnover of fC and caC by TDG-BER. PARylation of BER proteins is regulated by PARP and PARG activities. PARylation of BER proteins is important for DNA repair and chromatin association. PARylation of BER proteins interferes with DNA binding. PARylation of XRCC1 reduces DNA damage association in cells. PARylation promotes repair of DNA demethylation- and DNA damage-associated SSBs. PARylation is necessary for recruitment of DNA damage response factors to sites of spontaneous DNA damage. PARylation is required for turnover of engaged BER/SSBR. PARylation has a dual role in promoting enzymatic turnover in active DNA demethylation and in SSBR. PARylation is an integral part of targeted BER in the context of active DNA demethylation, where it regulates the coordinated action of TDG and the BER proteins. PARylation is a general feature of BER, as several DNA glycosylases are also PARylated following exposure to oxidative stress. PARylation controlled assembly and disassembly of protein complexes provide a mechanistic framework to explain the coordination and dynamics of complex multi-enzyme transactions involved in DNA repair and the maintenance of genomic function.