The Irre Cell Recognition Module (IRM) is an evolutionarily conserved group of transmembrane glycoproteins required for cell–cell recognition and adhesion in metazoan development. In Drosophila melanogaster ovaries, four members of this group – Roughest (Rst), Kin of irre (Kirre), Hibris (Hbs) and Sticks and stones (Sns) – play important roles in germ cell encapsulation and muscle sheath organization during early pupal stages, as well as in the progression to late oogenesis in the adult. Females carrying some of the mutant rst alleles are viable but sterile, and previous work from our laboratory had identified defects in the organization of the peritoneal and epithelial muscle sheaths of these mutants that could underlie their sterile phenotype. In this study, besides further characterizing the sterility phenotype associated with rst mutants, we investigated the role of the IRM molecules Rst, Kirre and Hbs in maintaining the functionality of the ovarian muscle sheaths. We found that knocking down any of the three genes in these structures, either individually or in double heterozygous combinations, not only decreases contraction frequency but also irregularly increases contraction amplitude. Furthermore, these alterations can significantly impact the morphology of eggs laid by IRM-depleted females demonstrating a hitherto unknown role of IRM molecules in egg morphogenesis.