Plant architecture is a major motif in plant diversity. The shape of the plant is regulated by genes that have been found to have similar or related functions in different species. However, changes in gene regulation or their recruitment to additional developmental pathways contribute to the wide range of plant patterns. Our aim was to unravel the genetic mechanisms governing the unique architecture of pepper (Capsicum annuum) and to determine whether these genetic factors have conserved functions in other plant species. We describe the pepper CaBLIND (CaBL) gene that is orthologous to the tomato (Solanum lycopersicum) BLIND (BL) and to the Arabidopsis thaliana REGULATOR OF AXILLARY MERISTEMS (RAX). We identified two allelic Cabl mutants that show dramatic reduction in axillary meristem initiation. In addition, Cabl exhibits late flowering and ectopic vegetative growth during the reproductive phase. Double-mutant and expression analyses suggest that CaBL functions independently of FASCICULATE, the pepper ortholog of SELF PRUNING in regulating sympodial growth, but is epistatic to FASCICULATE in controlling axillary meristem formation. Furthermore, CaBL operates independently of CaREVOLUTA and CaLATERAL SUPPRESSOR in regulating axillary branching. Our results provide evidence of CaBL's conserved function with BL and RAX genes in regulating axillary meristem initiation early in development. In addition, similar to BL but opposite to RAX, CaBL acts to promote the transition from vegetative to reproductive phase. However, in contrast to BL and RAX, CaBL is co-opted to play a role in suppressing vegetative growth during the reproductive phase in pepper.