MicroRNAs (miRNAs), a class of non-coding small RNAs, are crucial regulatory factors in plants and animals at the post-transcriptional level. These tiny molecules suppress gene expression by complementary oligonucleotide binding to sites in the target messenger. Recently, the discovery of plant-derived miRNAs with cross-kingdom abilities to regulate gene expression in insects has promoted exciting discussion, although some controversies exist regarding the modulation of insect development by plant-derived miRNAs. Here, we review current knowledge about the mechanisms of miRNA biogenesis, the roles of miRNAs in coevolution between insects and plants, the regulation of insect development by plant-derived miRNAs, the cross-kingdom transport mechanisms of plant-derived miRNAs, and cross-kingdom regulation. In addition, the controversy regarding the modulation of insect development by plant-derived miRNAs also was discussed. Our review provides new insights for understanding complex plant–insect interactions and discovering new strategies for pest management and even crop genetic improvement.