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DEAD-box protein 6 (DDX6) is a member of the DDX RNA helicase family that exists in all eukaryotes. It has been extensively studied in yeast and mammals and has been shown to be involved in messenger ribonucleoprotein assembly, mRNA storage, and decay, as well as in miRNA-mediated gene silencing. DDX6 participates in many developmental processes but the biological function of DDX6 in insects has not yet been adequately addressed. Herein, we characterized the <i>LmDDX6</i> gene that encodes the LmDDX6 protein in <i>Locusta migratoria</i>, a global, destructive pest. LmDDX6 possesses five motifs unique to the DDX6 subfamily. In the phylogenetic tree, LmDDX6 was closely related to its orthologs in <i>Apis dorsata</i> and <i>Zootermopsis nevadensis</i>. RT-qPCR data revealed high expression of <i>LmDDX6</i> in the ovary, muscle, and fat body, with a declining trend in the ovary after adult ecdysis. <i>LmDDX6</i> knockdown downregulated the expression levels of the juvenile hormone receptor <i>Met,</i> and genes encoding Met downstream targeted <i>Grp78-1</i> and <i>Grp78-2</i>, reduced <i>LmVg</i> expression, and impaired ovary development and oocyte maturation. These results demonstrate that <i>LmDDX6</i> plays an essential role in locust female reproduction and, thus, could be a novel target for locust biological control.