Precise control of gene expression is a hallmark of early development. To understand how random molecular interactions generate reproducible gene expression patterns, we have developed methods for absolute quantification of transcription rates. We examine gene expression dynamics at the level of individual gene loci using a combination of single molecule counting, live transcription imaging, and computer simulations. Several genes found in broad domains of the blastoderm stage embryo are expressed at equivalent rates within their respective domains of fastest accumulation. However, this fastest, or maximum, expression rate does not result from constitutive, fully active expression. Instead, transcription switches between expressing and non-expressing states during interphase, a phenomenon referred to as "bursting." Our analysis suggests that a single rate-limiting molecular interaction, occurring at random, determines bursting kinetics. We find that the on- and off-rates that determine bursting kinetics are finely tuned across genes in order to generate equivalent expression rates within domains of highest activity. We also find that a minimal promoter/enhancer from the gene hunchback is sufficient to confer bursting kinetics that are identical to those observed for the endogenous hunchback gene in the domain of highest activity. This suggests that multiple enhancers are not required to determine correct transcription dynamics.