To assess miRNA evolution across the Drosophila genus, we generated a comparative small RNA catalog of unprecedented breadth and depth for 12 fruitfly species. Aggregate analysis of several billion sRNA reads across multiple tissue types permits holistic miRNA annotations. Amongst well-conserved miRNAs, we observe unexpected cases of clade-specific variation in 5' end precision, occasional antisense loci, and putatively non-canonical loci. We also employ strict criteria to identify a massive set (649) of novel, evolutionarily-restricted miRNAs. Amongst the bulk collection of species-restricted miRNAs, two notable subpopulations are splicing-derived mirtrons and testis-restricted, clustered (TRC) canonical miRNAs. We quantify rates of miRNA birth and death using our annotation and a phylogenetic model for estimating rates of miRNA turnover in the presence of annotation uncertainty. Moreover, we define distinct molecular rationales associated with mirtrons and TRC miRNA evolution. Altogether, these data reveal miRNA diversity amongst Drosophila species and principles underlying their emergence and evolution.