Significance In most biological processes, genes have to be activated and/or repressed. In plants, the TOPLESS protein is essential for gene repression through its action as a corepressor bridging transcription factor with chromatin remodeling complexes. Here we combine biochemical and structural studies to describe the structure of TOPLESS, how it tetramerizes, and how it interacts with its protein partners. We show that both the tetramerization interface and the binding site for protein partners have been conserved since algae, highlighting the ancestrality of TOPLESS function. Comparison of this plant protein with one of its animal counterparts also shows how corepressors can use a common domain differently to achieve similar properties, illustrating the tinkering of evolution in transcriptional repression.