TATA box recognition by TATA-binding protein (TBP) is a key step in transcriptional initiation complex assembly on TATA-box-containing RNA polymerase (Pol) II and III promoters. This process is inhibited by the inhibitory DNA-binding (IDB) surface on the human TBP core domain (TBP(CORE)) and is stimulated by promoter-specific basal transcription factors, such as two human TFIIB family members, the Pol II factor TFIIB and the Pol III factor Brf2, which is required for transcription from TATA-box-containing Pol III promoters. In contrast, the third TFIIB family member, Brf1, which is required for transcription from TATA-less Pol III promoters, does not stimulate TBP binding to the TATA box. We show here that in addition to its role in regulating TBP binding to a TATA box, the TBP IDB surface is unexpectedly involved in TBP association with all three TFIIB family members. Interestingly, the loss of IDB function has specific and diverse effects on each TFIIB family member. Indeed, the IDB and prototypical TFIIB contact surfaces of TBP, which lie on opposite sides of the TBP(CORE), cooperate to form the wild-type TFIIB-TBP-TATA box complex. These results reveal how, through differential usage of opposite surfaces of the TBP(CORE), TBP can achieve versatility in the assembly of Pol II and Pol III promoter complexes with TFIIB family proteins.