The genus Asparagus is unusual in producing axillary, determinate organs called cladodes, which may take on either a flattened or cylindrical form. Here, we investigated the evolution of cladodes to elucidate the mechanisms at play in the diversification of shoot morphology. Our observations of Asparagus asparagoides, which has leaf-like cladodes, showed that its cladodes are anatomically and developmentally similar to leaves but differ in the adaxial/abaxial polarity of the vasculature. In addition to the expression of an ortholog of KNAT1, orthologous genes that are normally expressed in leaves, asymmetric leaves1 and HD-ZIPIII, were found to be expressed in cladode primordia in a leaf-like manner. The cylindrical cladodes of Asparagus officinalis showed largely similar expression patterns but showed evidence of being genetically abaxialized. These results provide evidence that cladodes are modified axillary shoots, suggest that the co-option of preexisting gene networks involved in leaf development transferred the leaf-like form to axillary shoots, and imply that altered expression of leaf polarity genes led to the evolution of cylindrical cladodes in the A. officinalis clade.