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Abstract How recently originated gene copies become stable genomic components remains uncertain as high sequence similarity of young duplicates precludes their functional characterization. The tandem multigene familySdicis specific toDrosophila melanogasterand has been annotated across multiple reference-quality genome assemblies. Here we show the existence of a positive correlation betweenSdiccopy number and totalexpression, plus vast intrastrain differences in mRNA abundance among paralogs, using RNA-sequencing from testis of four strains with variable paralog composition. Single cell and nucleus RNA-sequencing data expose paralog expression differentiation in meiotic cell types within testis from third instar larva and adults. Additional RNA-sequencing across synthetic strains only differing in theirYchromosomes reveal a tissue-dependenttrans-regulatory effect onSdic: upregulation in testis and downregulation in male accessory gland. By leveraging paralog-specific expression information from tissue- and cell-specific data, our results elucidate the intraspecific functional diversification of a recently expanded tandem gene family.