In plant hormone signaling, transcription factor regulatory networks (TFRNs), which link the master transcription factors to the biological processes under their control, remain insufficiently characterized despite their crucial function. Here, we identify a TFRN involved in the response to the key plant hormone auxin and define its impact on auxin-driven biological processes. To reconstruct the TFRN, we developed a three-step procedure, which is based on the integrated analysis of differentially expressed gene lists and a representative collection of transcription factor binding profiles. Its implementation is available as a part of the CisCross web server. With the new method, we distinguished two transcription factor subnetworks. The first operates before auxin treatment and is switched off upon hormone application, the second is switched on by the hormone. Moreover, we characterized the functioning of the auxin-regulated TFRN in control of chlorophyll and lignin biosynthesis, abscisic acid signaling, and ribosome biogenesis.