The genome of the archaeon Halobacterium salinarum contains two copies of the pst (phosphate‐specific transport) operon, the genes of which are related to well‐studied bacterial homologues. Both operons (pst1 and pst2) were shown to be polycistronic and, when under Pi‐limited conditions, transcription initiated 1 bp upstream of the translational starts. Under Pi saturation, the pst1 operon utilized an additional transcription start site 59 bp upstream of the first one. The leaderless pst1 transcript was found to be more efficiently translated than the leadered transcript. Promoter strengths differed significantly between the two operons and when Pi levels changed. The basal pst1 promoter activity in Pi‐saturated conditions was minimal while the pst2 promoter was active. In contrast, phosphate limitation induced the pst1 operon threefold more than the pst2 operon. We identified basic and phosphate‐dependent cis‐acting elements in both promoters. Phosphate‐uptake assays conducted with several Pst1 and Pst2 mutant strains revealed differences in the substrate affinities between the two transporters and also suggested that the Pi‐binding proteins PstS1 and PstS2 can interact with either of the two permease subunits of the transporters. The tactic behaviour of wild type and pst‐deletion strains showed that the Pst1 transporter plays an important role for phosphate‐directed chemotaxis.