Updated project metadata. Base excision repair (BER) initiated by alkyladenine DNA glycosylase (AAG; aka MPG) is essential for removal of aberrantly methylated DNA bases. Genome instability and accumulation of aberrant bases accompany multiple diseases including cancer and neurological disorders. While BER is well studied on naked DNA, it is currently unclear how BER efficiently operates on chromatin. Here we show that AAG binds to chromatin and forms a complex with active RNA polymerase (pol) II. This occurs through direct binding to Elongator and results in co-regulation of gene expression. Interestingly, endogenous aberrantly methylated bases accumulate at 3’end of co-regulated genes, in regions enriched for Elongator, active RNA pol II, and BER enzymes AAG and APE1. Active transcription and functional Elongator are further vital to ensure efficient BER by promoting AAG and APE1 chromatin occupancy. Our findings indicate that AAG needs to associate with transcription elongation to maintain genome stability, concurrently coordinating repair with gene expression.