The budding yeast Shu complex is an obligate heterotetramer that promotes error-free homologous recombination by facilitating the assembly of Rad51 filaments on single-stranded DNA after the resection of a double-strand break. The Shu complex is composed of two Rad51 paralogs, Psy3 and Csm2, a third protein Shu1, and a SWIM domain containing protein called Shu2. Orthologs of the Shu complex are conserved among eukaryotes, and mutations in human Rad51 paralogs are associated with cancer predisposition and Fanconi anemia. We have been characterizing a novel function for the Shu complex in the repair of DNA alkylation damage during post-replicative repair (PRR). Here we uncover the interplay between the Shu complex members and base excision repair (BER) machinery upon MMS-induced alkylation damage, providing evidence for the Shu complex’s role in bypassing certain BER intermediates. Specifically, cells that lack the BER glycosylase MAG1, or the apurinic/apyrimidinic (AP) endonucleases APN1 and APN2, preferentially utilize HR to repair MMS damage. The increased HR observed in mag1∆ and apn1∆ apn2∆ cells is Shu complex dependent. Furthermore, mutation of the translesion polymerase REV3, which is involved in error-prone PRR, further sensitizes these cells to MMS in a shu∆ background. Our work illustrates a role for the Shu complex in the promotion of error-free DNA damage resolution in a replicative context and provides further evidence for its importance in maintaining genomic stability.