The complex spatial and temporal patterns of gene expression during development of multicellular organisms are determined by the binding of transcription factor proteins to regions of genomic DNA called enhancers. Traditionally, tests of the in vivo functions of transcription factors have been performed using modified native enhancers. These native enhancers have provided great insight, but can also yield unpredictable results, presumably because they also encode sites of unknown function. A synthetic, transcriptionally silent enhancer platform may allow cleaner tests of regulatory protein function, but, to date, attempts to build a synthetic enhancer in a multicellular eukaryote—by combining binding sites for transcriptional activators and repressors—have largely failed to produce predictable patterns of gene expression. Here we report construction of a fully synthetic transcriptional platform in Drosophila consisting of an engineered transcriptional activator and an artificial enhancer platform. We found that binding sites for a transcriptional activator are not sufficient to drive transcription. Instead, binding sites for a transcription factor that makes DNA accessible are required together with binding sites for transcriptional activators to produce a functional enhancer. Only in this context can changes in the number of activator binding sites mediate quantitative control of transcription. Our synthetic system provides a platform for testing models of transcriptional regulation and will provide an improved understanding of how natural networks function.