The human U2 snRNA promoter directs the formation of a specialized RNA polymerase II transcription complex that recognizes the snRNA gene 3' box as a signal for RNA 3' end formation. In contrast, the human U6 promoter is recognized by RNA polymerase III and transcription terminates in a run of Ts. We show that transcription from the U6 promoter is dependent on a sequence similar to the U2 proximal element and on an AT-rich element centered around position -27. Mutation of the AT-rich element induces RNA polymerase II transcription from the U6 promoter, whereas insertion of this element within the U2 promoter converts it into a predominantly RNA polymerase III promoter. The site of transcription termination always correlates with the nature of the transcribing polymerase: the 3' box with RNA polymerase II and a run of Ts with RNA polymerase III. Thus, a single element determines the RNA polymerase specificity of snRNA promoters and hence the site of transcription termination.