In this article, we identify and characterise the miRNA machinery components Drosha, Dicer-1 and Argonaute-1 of the desert locust. By means of phylogenetic analyses, we reveal important insights in the evolutionary context of these components. Our data illustrate that insect Argonaute-1 proteins form a monophyletic group with ALG-1 and ALG-2 of Caenorhabditis elegans and with the four (non-Piwi) Argonaute proteins present in humans. On the other hand, humans apparently lack clear homologues of the insect Argonaute-2 proteins. In addition, we demonstrate that drosha, dicer-1 and argonaute-1 display wide transcript tissue-distribution in adult desert locusts, and that during locust phase transition and feeding of starved locusts the expression levels of the miRNA pathway are regulated at the transcript level.