The pearl oyster, Pinctada radiata, shows great variation in shell morphology throughout its distribution. This variation can be related to phenotypic plasticity, genetic variability or a combination of both. Using geometric morphometric and microsatellite DNA analyses, two morphologically distinct populations of the pearl oyster were studied in the northern Persian Gulf, i.e. from the Lavan and Hendourabi Islands. Ten landmarks were selected to define the shape of the left shell. In addition, concentration of Zn, Mg, Fe, Cu, Pb, Cd, Mn and Cr of the soft tissues were measured using atomic absorption spectrometry. Six microsatellite loci were used to assess the population genetic structure of the pearl oyster. There were morphometric differences between the populations suggesting the existence of two morphotypes. There was a significant difference between the two populations in concentrations of Fe, Mg, Zn, Cd, Mn and Cr indicating that the specimens from the Lavan Island experience a more stressful environment than those from the Hendourabi Island. Analysis of molecular variance (AMOVA) indicated that the proportion of the genetic variation attributed to differences among populations of the pearl oyster was highly significant for both FST and RST (FST = 0.066, RST = 0.265, P < 0.001). Our findings showed that stressful conditions resulting from heavy metals may have a direct influence on the separation of the populations in Lavan and Hendourabi despite the lack of a physical barrier.