This study attempted to determine short-term responses to drought and salt stress in different Silene vulgaris genotypes and to identify potential abiotic stress biochemical indicators in this species. Four populations from contrasting habitats were subjected to drought and three levels of salinity under controlled greenhouse conditions. The determination of several growth parameters after the stress treatments allowed for ranking the tolerance to stress of the four analyzed populations on the basis of their relative degree of stress-induced growth inhibition. This was then correlated with changes in the leaf levels of monovalent ions (Na+, Cl−, and K+), photosynthetic pigments (chlorophylls a and b, carotenoids), osmolytes (total soluble sugars, proline), and non-enzymatic antioxidants (total phenolic compounds and flavonoids). Despite the observed differences, all four populations appeared to be relatively tolerant to both stress conditions, which in general did not cause a significant degradation of photosynthetic pigments and did not generate oxidative stress in the plants. Drought and salinity tolerance in S. vulgaris was mostly dependent on the use of Na+ and K+ for osmotic adjustment under stress, a mechanism that appeared to be constitutive, and not stress-induced, since relatively high concentrations of these cations (without reaching toxic levels) were also present in the leaves of control plants. The inhibition of additional transportation of toxic ions to the leaves, in response to increasing external salinity, seemed to be a relevant mechanism of tolerance, specifically to salt stress, whereas accumulation of soluble sugars under drought conditions may have contributed to tolerance to drought.