The LIM-domain-only protein-4 (LMO4), which consists only of two protein-interacting zinc fingers, is indispensable in embryonic development and is overexpressed in >50% of non hereditary breast cancers. Its interaction partners have diverse functions including controlling the cell cycle, signal transduction and regulating transcription. One of these partners is Deformed Epidermal Autoregulatory Factor-1 (DEAF1), a modular transcription factor that is co-expressed with LMO4 in neurons, breast epithelial cells, the pancreas and lungs. Similar phenotypes result when either protein is overexpressed or knocked-out, implying that LMO4 and DEAF1 functions as a complex in cells. Thus we aimed to characterize the LMO4-DEAF1 interaction. The LMO4-binding domain in DEAF1 lies adjacent to a nuclear export signal (NES). We show that the NES is embedded within a tetrameric coiled coil domain. We mapped the residues on each protein that are important for complex formation. DEAF1 preferentially binds the C-terminal LIM domain of LMO4 (LMO4LIM2). The solution structure of the LMO4LIM2-DEAF1 intramolecular complex shows that the proteins bind in a head-to-tail manner and that the DEAF1 LIM-interacting domain (DEAF1LID) binds LMO4LIM2 in an extended conformation. We show that DEAF1LID becomes ordered upon binding LMO4LIM2 and that the glycine-serine peptide linker used to tether LMO4LIM2 to DEAF1LID is flexible, thus allowing a native-like complex to form. The surface on LMO4 bound by DEAF1 is also bound by LDB1, a co-factor of nuclear LIM domain proteins, and the tumour suppressor CtIP, which is involved in DNA repair. We hypothesize that under normal circumstances competition for binding to LMO4 integrates diverse cellular pathways, and that disease results from perturbing concentrations of LMO4 and its binding partners.