The study presents the miRNA profiles of two Indian sheep populations with divergent carcass and muscle traits. The RNA sequencing of longissimus thoracis muscles from the two populations revealed a total of 400 known miRNAs. Myomirs or miRNAs specific to skeletal muscles identified in our data included oar-miR-1, oar-miR-133b, oar-miR-206 and oar-miR-486. Comparison of the two populations led to identification of 100 differentially expressed miRNAs (p < 0.05). A total of 45 miRNAs exhibited a log fold change of ≥ ( ±) 3.0. Gene Ontology analysis revealed cell proliferation, epithelial to mesenchymal transition, apoptosis, immune response and cell differentiation as the most significant functions of the differentially expressed miRNAs. The differential expression of some miRNAs was validated by qRT-PCR analysis. Enriched pathways included metabolism of proteins and lipids, PI3K-Akt, EGFR and cellular response to stress. The microRNA-gene interaction network revealed miR-21, miR-155, miR-143, miR-221 and miR-23a as the nodal miRNAs, with multiple targets. MicroRNA-21 formed the focal point of the network with 42 interactions. The hub miRNAs identified in our study form putative regulatory candidates for future research on meat quality traits in Indian sheep. Our results provide insight into the biological pathways and regulatory molecules implicated in muscling traits of sheep.