MicroRNAs are short non-protein coding RNAs which negatively regulate gene expression by guiding the RNA-induced silencing complex to complementary target mRNAs. MicroRNA regulation is implicated in essentially all biological processes, and microRNAs have a prominent role in animal development. Several microRNA families are conserved between deuterostomes and protostomes, however the majority of microRNAs in animal species are a result of continuous de novo gene birth processes throughout natural history. The acquisition of novel microRNAs, and changes in existing microRNAs, has been suggested to play a role in animal evolution. However, the constraints on microRNA emergence, evolution and expression are not well understood. We have studied the interplay of microRNA developmental expression and evolutionary dynamics in model insects displaying different modes of embryogenesis. We first determined the evolutionary origins and rates of change of microRNAs in Drosophila melanogaster and Drosophila virilis, and analysed their temporal expression profiles throughout development by deep sequencing. We found a good correlation between microRNA conservation and abundance at most stages except for the early embryo, where fast-evolving microRNAs are highly expressed. We further showed that the temporal expression of orthologous microRNAs is highly similar between species, and the global microRNA profiles across development display an hourglass-like conservation pattern, previously observed for protein-coding genes. We next extended our analyses to the red flour beetle Tribolium castaneum, which develops via the short germband mode of embryogenesis. This developmental mode is ancestral and widespread in arthropods, yet the microRNA complement of a representative species has not been previously characterized. We find a number of conserved features between Drosophila and Tribolium, including microRNA maternal loading and modifications, and microRNA-mediated targeting of maternally deposited transcripts. We also describe an abundant pool of maternally loaded and zygotically expressed piRNAs, which appear to be turned on in response to active transposons. In contrast to the previously observed piRNA profile in flies, beetle piRNAs are abundant throughout the entire embryogenesis. A majority of the newly identified microRNAs in the flour beetle are expressed during a discrete period in the early blastoderm, and also target maternally provided transcripts. The observation that the early embryos of both Drosophila and Tribolium are uniquely characterized with high levels of novel and dynamically evolving microRNAs suggests a conserved phenomenon where the blastoderm stage is a highly permissive environment for microRNA innovations.