Drosophila egg development is an established model for studying epithelial patterning and morphogenesis, but the connection between signaling pathways and egg morphology is still incompletely understood. We have identified a non-classical cadherin, Cad74A, as a putative adhesion gene that bridges epithelial patterning and morphogenesis in the follicle cells. Starting in mid-oogenesis, Cad74A is expressed in the follicle cells that contact the oocyte, including the border cells and most of the columnar follicle cells. However, Cad74A is repressed in two dorsolateral patches of follicle cells, which participate in the formation of tubular respiratory appendages. We show genetically that Cad74A is downstream of the EGFR and BMP signaling pathways and is repressed by the Zn-finger transcription factor Broad. The correlation of Cad74A repression in the cells that bend out of the plane of the follicular epithelium is preserved across Drosophila species and mutant backgrounds exhibiting a range of eggshell phenotypes. Complete removal of Cad74A from the follicle cells causes defects in dorsal appendage formation. Ectopic expression of Cad74A in the roof cells results in shortened, flattened appendages due to the hindered migration of the roof cells. Based on these results, we propose that Cad74A is part of the adhesive machinery that enables robust dorsal appendage formation, and as such provides a link between the patterning of the follicle cells and eggshell morphogenesis.