The salmon louse Lepeophtheirus salmonis is a marine ectoparasite that has a detrimental impact on salmon farms. Genomic knowledge of adult stages is critical to understand the reproductive success and lifecycle completion of this species. Here, we report a comprehensive characterization of the L. salmonis miRNome with emphasis on the sex-differences of the parasite. Small-RNA sequencing was conducted on males and females, and mRNA-sequencing was also conducted to identify miRNA-targets at these stages. Based on bioinformatics analyses, 3101 putative miRNAs were found in L. salmonis, including precursors and variants. The most abundant and over-expressed miRNAs belonged to the bantam, mir-100, mir-1, mir-263a and mir-276 families, while the most differentially expressed mRNAs corresponded to genes related to reproduction and other biological processes involved in cell-differentiation. Target analyses revealed that the most up-regulated miRNAs in males can act by inhibiting the expression of genes related to female differentiation such as vitellogenin genes. Target prediction and expression patterns suggested a pivotal role of miRNAs in the reproductive development of L. salmonis.