Histone mRNA encodes proteins essential for genome packaging, and their abundance must be tightly controlled to maintain genome integrity. While histone mRNAs are degraded in dividing cells in a cell cycle-dependent manner, how they are regulated in non-dividing cells remains poorly understood. Here, we used post-meiotic male germ cells to investigate histone mRNA turnover during sperm development. We identify the histone variant H2A.B.3 as a chromatin-linked regulator of a previously unrecognized nuclear pathway for selective histone mRNA degradation. H2A.B.3 associates with histone mRNAs and nuclear RNA processing machinery to promote histone mRNA decay. Mechanistically, H2A.B.3 recognizes the stem-loop structure of replication-dependent (RD) histone mRNAs and facilitates the recruitment of phosphorylated UPF1 (phUPF1) in an RNA-dependent manner, promoting their degradation by the nuclear exosome. Loss of H2A.B.3 causes aberrant stabilization of histone mRNAs in haploid germ cells, whereas ectopic H2A.B.3 expression accelerates histone mRNA degradation. Depletion of UPF1 abolishes the effect of H2A.B.3-mediated histone mRNA decay, demonstrating that UPF1 is an essential downstream effector of this pathway. These findings reveal a previously unrecognized nuclear function of H2A.B.3 as a molecular link between chromatin regulation and selective histone mRNA surveillance. Collectively, our study uncovers a chromatin-guided mechanism of histone mRNA turnover required for proper histone-protamine exchange, sperm chromatin remodeling, and male fertility, with broader implications for histone variant-mediated RNA metabolism in development and disease, including malignancies.