DNA polymerase delta (Pol δ) plays a critical role in transferring parental histones to the lagging strand during DNA replication, ensuring the faithful inheritance of epigenetic information. The study identifies Pol32, a nonessential subunit of Pol δ, as a key histone chaperone that facilitates the transfer of parental histone H3–H4 to the lagging strand. Pol32 binds to histone H3–H4 both in vivo and in vitro, and its interaction with histones is dependent on Mcm2. Depletion of Pol32 results in a predominant transfer of parental histone H3–H4 to the leading strand, highlighting its essential role in lagging strand histone transfer. Pol32 acts downstream of Mcm2 and upstream of DNA polymerase α (Pol1), forming a pathway for parental histone H3–H4 transfer. The study also shows that Pol32 functions independently of its interaction with PCNA and DNA binding capability, emphasizing its role as a histone chaperone. The findings reveal a molecular mechanism for parental histone transfer, a crucial step in epigenetic inheritance. The study underscores the importance of DNA polymerase complexes in chromatin replication and epigenetic stability, with implications for chromatin instability and cell fate determination. The results provide insights into the regulatory mechanisms of histone transfer and highlight the significance of Pol32 in maintaining epigenetic information during DNA replication.DNA polymerase delta (Pol δ) plays a critical role in transferring parental histones to the lagging strand during DNA replication, ensuring the faithful inheritance of epigenetic information. The study identifies Pol32, a nonessential subunit of Pol δ, as a key histone chaperone that facilitates the transfer of parental histone H3–H4 to the lagging strand. Pol32 binds to histone H3–H4 both in vivo and in vitro, and its interaction with histones is dependent on Mcm2. Depletion of Pol32 results in a predominant transfer of parental histone H3–H4 to the leading strand, highlighting its essential role in lagging strand histone transfer. Pol32 acts downstream of Mcm2 and upstream of DNA polymerase α (Pol1), forming a pathway for parental histone H3–H4 transfer. The study also shows that Pol32 functions independently of its interaction with PCNA and DNA binding capability, emphasizing its role as a histone chaperone. The findings reveal a molecular mechanism for parental histone transfer, a crucial step in epigenetic inheritance. The study underscores the importance of DNA polymerase complexes in chromatin replication and epigenetic stability, with implications for chromatin instability and cell fate determination. The results provide insights into the regulatory mechanisms of histone transfer and highlight the significance of Pol32 in maintaining epigenetic information during DNA replication.