Gene duplications are considered to be the major evolutionary resource of novel functions. The gene family Esf2/ABP1 is conserved in metazoan organisms from yeast to humans. Here we performed a search and characterization of Esf2/ABP1 homologs in the Drosophila genus. Whereas in the majority of Drosophila species this gene family is represented by only a single gene, in the melanogaster and suzukii subgroups recurrent gene duplications arose, providing 47 homologous genes located on the X chromosome. To study the evolutionary history of duplicates, we performed phylogenetic, functional domain, and tissue-specific expression analyses. We revealed a male-specific and testis-biased transcription pattern of duplicated copies in Drosophila melanogaster and Drosophila sechellia compared to ubiquitous expression of the parental gene. The amplification of 21 repeated paralogs within the heterochromatic piRNA cluster resulted in the ovarian-specific transformation of these repeats into piRNAs in D. melanogaster. In three species of the suzukii subgroup, Esf2/ABP1 genes evolved with domain diversification: in addition to RNA-binding ABT1-like domain preservation, all homologous proteins acquired expanded intrinsically disordered regions. By studying the duplicated copies of the Esf2/ABP1 family in Drosophila, we offer insight into how novel gene functions emerge and are maintained, contributing to life's diversity and complexity.