<i>Background:</i> Thus far the search for osteoporosis candidate genes has focused less attention on the regulation of calcium homeostasis. Associations of vitamin D receptor (VDR) <i>FokI</i>, calcium-sensing receptor (CaSR) <i>A986S</i> and parathyroid hormone (PTH) <i>BstBI</i> polymorphisms with calcium homeostasis and peripheral bone density were investigated in adult Finns. <i>Methods:</i> The subgroup of the population-based FINRISK survey consists of 339 healthy adults aged 31–43 years. Lifestyle data were assessed with questionnaires and food diaries. DNA was isolated from blood, and biochemical determinants of calcium metabolism were measured from blood and 24-hour urine samples. Bone mineral density (BMD) was measured using the DXA method at the distal forearm and by quantitative ultrasound (broadband ultrasound attenuation and speed of sound) at the calcaneus. Subjects were genotyped for VDR <i>FokI</i>, CaSR <i>A986S</i> and PTH <i>BstBI</i> polymorphisms. <i>Results:</i> The CaSR <i>986S</i> allele was associated with higher serum ionized calcium (p = 0.014). Forearm BMD was lowest for the PTH <i>BstBI</i> genotype <i>bb</i> in males (p = 0.023). VDR <i>FokI</i> and PTH <i>BstBI</i> polymorphisms showed a significant interaction on serum PTH (p = 0.010). The other gene–gene or diet–gene interactions studied showed no significant results. <i>Conclusions:</i> VDR, CaSR and PTH contribute to the genetic regulation of calcium homeostasis and peripheral bone density.