Fruit ripening is a complex developmental process responsible for the transformation of the seed-containing organ into a tissue attractive to seed dispersers and agricultural consumers. The coordinated regulation of the different biochemical pathways necessary to achieve this change receives considerable research attention. The MADS-box transcription factor RIPENING INHIBITOR (RIN) is an essential regulator of tomato (Solanum lycopersicum) fruit ripening but the exact mechanism by which it influences the expression of ripening-related genes remains unclear. Using a chromatin immunoprecipitation approach, we provide evidence that RIN interacts with the promoters of genes involved in the major pathways associated with observed and well-studied ripening phenotypes and phenomena, including the transcriptional control network involved in overall ripening regulation, ethylene biosynthesis, ethylene perception, downstream ethylene response, cell wall metabolism, and carotenoid biosynthesis. Furthermore, in the cases of ethylene and carotenoid biosynthesis, RIN interacts with the promoters of genes encoding rate-limiting activities. We also show that RIN recruitment to target loci is dependent on a normally functioning allele at the ripening-specific transcription factor COLORLESS NONRIPENING gene locus, further clarifying the relationship between these two ripening regulators.