Auxin is an essential regulator of virtually all aspects of plant growth and development and components of the auxin signaling pathway are conserved among land plants. Yet, a remarkable degree of natural variation in physiological and transcriptional auxin responses has been described among Arabidopsis thaliana accessions. Such variations might be caused by divergence in promoter or coding sequences of signaling and/or response genes that ultimately result in altered protein levels or functions. As intra-species comparisons offer only limited sequence variation, we here combined physiological, transcriptomic and genomic information to inspect the variation of auxin responses between A. thaliana and A. lyrata. This approach allowed the identification of genes with conserved auxin responses in both species and provided novel genes with potential relevance for auxin biology. Furthermore, gene expression and promoter sequence divergence were exploited to assess putative sources of variation. De novo motif discovery identified variants of known as well as novel promoter elements with potential relevance for transcriptional auxin responses. Furthermore, expression of AUXIN/INDOLE-3-ACETIC ACID (AUX/IAA) signaling genes was highly diverse between A. thaliana and A. lyrata. Network analysis revealed positive and negative correlations of inter-species differences in the expression of AUX/IAA gene clusters and classic auxin-related genes. We conclude that variation in general transcriptional and physiological auxin responses may originate substantially from functional or transcriptional variations in the TRANSPORT INHIBITOR RESPONSE 1/AUXIN SIGNALING F-BOX, AUX/IAA and AUXIN RESPONSE FACTOR signaling network. In that respect, AUX/IAA gene expression divergence potentially reflect differences in the manner in which different species transduce identical auxin signals into gene expression responses.