MicroRNA (miRNA)-guided post-transcriptional regulation is an important mechanism of gene regulation during multiple biological processes including response to abiotic stresses. Foxtail millet is a model crop, which is genetically closely related to several bioenergy grasses and also known for its potential abiotic stress tolerance. Hence deciphering the role of miRNAs in regulating stress-responsive mechanism would enable imparting durable stress tolerance in both millets and bioenergy grasses. Considering this, a comprehensive genome-wide in silico analysis was performed in foxtail millet which identified 355 mature miRNAs along with their secondary structure as well as corresponding targets. Predicted miRNA targets were found to encode various DNA binding proteins, transcription factors or important functional enzymes, which could be the crucial regulators in plant abiotic stress responses. All the 355 miRNAs were physically mapped onto the foxtail millet genome and in silico tissue-specific expression for these miRNAs were studied. Comparative mapping of the 355 miRNAs between foxtail millet and other related grass species would assist miRNA studies in these genetically closely-related plants. Expression profiling was performed for eight candidate miRNAs under diverse abiotic stresses in foxtail millet, which unravelled the putative involvement of these miRNAs in stress tolerance. With an aim of providing the generated miRNA marker information to the global scientific community, a foxtail millet MiRNA Database (FmMiRNADb: http://18.104.22.168/FmMiRNADb/index.html) has also been constructed. Overall, the present study provides novel insights onto the role of miRNAs in abiotic stress tolerance and would promisingly expedite research on post-transcriptional regulation of stress-related genes in millets and bioenergy grasses.