Butterflies have evolved different colour patterns on their dorsal and ventral wing surfaces to serve different signalling functions, yet the developmental mechanisms controlling surface-specific patterning are still unknown. Here, we mutate both copies of the transcription factor <i>apterous</i> in <i>Bicyclus anynana</i> butterflies using CRISPR/Cas9 and show that <i>apterous A,</i> expressed dorsally, functions both as a repressor and modifier of ventral wing colour patterns, as well as a promoter of dorsal sexual ornaments in males. We propose that the surface-specific diversification of wing patterns in butterflies proceeded via the co-option of <i>apterous A</i> or its downstream effectors into various gene regulatory networks involved in the differentiation of discrete wing traits. Further, interactions between <i>apterous</i> and sex-specific factors such as <i>doublesex</i> may have contributed to the origin of sexually dimorphic surface-specific patterns. Finally, we discuss the evolution of eyespot number diversity in the family Nymphalidae within the context of developmental constraints due to <i>apterous</i> regulation