Salt cress (Eutrema salsugineum) presents relatively high phosphate (Pi) use efficiency cy in its natural habitat. Phosphate Transporters (PHTs) play critical roles in Pi acquisition and homeostasis. Here, a comparative study of PHT families between salt cress and Arabidopsis was performed. A total of 27 putative PHT genes were identified in E. salsugineum genome. Notably, seven tandem genes encoding PHT1;3 were found, and function analysis in Arabidopsis indicated at least six EsPHT1;3s participated in Pi uptake. Meanwhile, different expression profiles of PHT genes between the two species under Pi limitation and salt stress were documented. Most PHT1 genes were down‐regulated in Arabidopsis while up‐regulated in salt cress under salinity, among which EsPHT1;9 was further characterized. EsPHT1;9 was involved in root‐to‐shoot Pi translocation. Particularly, the promoter of EsPHT1;9 outperformed that of AtPHT1;9 in promoting Pi translocation, K⁺/Na⁺ ratio, thereby salt tolerance. Through cis‐element analysis, we identified a bZIP transcription factor EsABF5 negatively regulating EsPHT1;9 and plant tolerance to low‐Pi and salt stress. Altogether, more copies and divergent transcriptional regulation of PHT genes contribute to salt cress adaptation to the co‐occurrence of salinity and Pi limitation, which add our knowledge on the evolutionary and molecular component of multistress‐ tolerance of this species.