Auxin is a phytohormone involved in a wide range of developmental processes. Whilst auxin-mediated signalling is now known to occur through a range of pathways, the transduction of auxin signalling within the carpels has mainly been studied in the context of the ETTIN (ETT) mediated pathway. Several lines of evidence suggest a role for the canonical TIR1/AFB2-mediated pathway in carpel development. However, the relationship between canonical and ETT-mediated mechanisms has not been investigated. Here,tir1-1 afb2-3 ett-3triple mutants were generated inArabidopsis, and phenotypic analysis showed synergism between the canonical and ETT-mediated pathways in gynoecium development. Furthermore, ETT shares partial redundancy with ARF4, a close paralog which interacts with the canonical pathway AUX/IAAs. However, the role of ARF4 in the regulation of auxin-responsive gene expression has not been studied in the gynoecium. Here comparative transcriptomics were utilized to assess the roles of ETT and ARF4 in gynoecium development, and the mis-regulation of the auxin response inett-3 arf4-2mutants. The data suggest that the auxin independent mis-regulation ofYABBY2, YABBY5, andCRABSCLAWcontributes to the abaxial-adaxial identity defects observed in gynoecia and leaves of the double mutant. Auxin sensitive transcriptomics analyses suggest that ETT and ARF4 maintain the auxin insensitivity of both distinct and overlapping targets, many of which become upregulated by auxin in their absence. This is consistent with previously proposed models of A-B ARF antagonism, and suggests that the maintenance of auxin insensitivity at target loci may play an equally important role as the auxin-sensitive induction of genes for a range of developmental processes.