Spermatogenesis is a complex process where spermatogonia differentiate into haploid sperm cells. Genes guiding this process are subject to an evolutionary trade-off between purifying selection preserving basic functions and positive selection favoring fast gamete production and innovative sperm traits. The outcome of this trade-off varies across the spermatogenesis stages in mammals but remains unexplored for species with ZW sex chromosomes, such as birds. Here we identify 20 cell clusters comprising somatic and germline cells across stages of spermatogenesis by using single-cell RNA sequencing of collared and pied flycatcher testis. Based on an ortholog comparison with mammals, analyses of differential gene expression between two closely-related flycatcher species and lineage-specific protein sequence evolution, we find evidence for rapid divergence of genes expressed during the second and last major stages of spermatogenesis (meiosis and spermiogenesis). The genes that are differentially expressed between the two flycatcher species are enriched for Gene Ontology biological processes that are fundamental for sperm function. While genes expressed during spermiogenesis are known to evolve fast in mammals, our results imply that gene expression at meiosis are subject to stronger positive selection or is less constraint by purifying selection and/or by intralocus sexual conflict in birds as compared to mammals. We also find signals of fast evolving Z-linked genes expressed during meiosis, consistent with the lack of sex-chromosome silencing during meiosis (MSCI) in birds.