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Homeostasis of calcium (Ca) and phosphate (Pi) is maintained by a concerted interplay of absorption and reabsorption via the gastrointestinal tract and the kidney and by storage and mobilization from the bone regulated mainly by parathyroid hormone (PTH), 1,25‐dihydroxycholecalciferol and calcitonin. The present study aimed at characterizing the effects of dietary P restriction on bone, vitamin D metabolism and rumen fermentation traits reflecting the endogenous P cycle maintaining the ruminal P supply for microbial metabolism. The experiments were done in eleven female, non‐pregnant, non‐lactating four‐ to nine‐year‐old Black Headed Mutton sheep allotted to two feeding groups: "P‐restricted" (0.11% P/kg DM and 0.88% Ca/kg DM) and "Control" (0.38% P/kg DM and 0.88% Ca/kg DM). Dietary P restriction did not lead to hypophosphataemia, probably due to a compensation by bone mobilization, demonstrated by increased serum concentrations of a resorption marker and altered gene expression in bone tissue. In addition, the RNA expression of fibroblast growth factor 23, a bone‐derived factor involved in the regulation of vitamin D metabolism, was significantly reduced with dietary P restriction. Furthermore, several genes related to vitamin D metabolism and plasma concentrations of 1,25‐(OH)2D were associated with serum concentrations of phosphate (Pi). In the parotid gland, the expression of the Pi transporter NaPi2b was negatively associated with serum Pi and positively with parathyroid PTH expression. Although Pi concentrations in saliva and the gastrointestinal tract were significantly reduced, we found no adverse effects of the P‐restricted ration on the production of short chain fatty acids, but slight differences in the production of butyrate as well as its relationship to rumen Pi and ammonia concentrations that might indicate an impact on ruminal fermentation. [ABSTRACT FROM AUTHOR]