Genetic selection for high growth rate has resulted in tremendous changes not only in feed efficiency, but also in water consumption between modern broilers and their ancestor jungle fowl (JF). However molecular mechanisms involved in water homeostasis are still not well defined. This study aimed, therefore, to determine the effect of short-term water restriction on the expression of water channel- and noncoding RNA biogenesis-related genes in the kidney and whole blood of JF, broiler population from the 1990s (RB1995), and modern broiler population developed in 2015 (ARB2015). Body weight-matched birds from each population were subjected to water restriction (WR) for 3 h or had ad libitum access to water in a 3 × 2 factorial design. The expression of target genes was determined by real-time quantitative PCR. WR significantly reduced body weight in RB1995, but not in JF or ARB2015. In the kidney, WR up-regulated the expression of AQP2 in all chicken populations, AQP3 in the RB1995, and ATP1B1 in JF and ARB2015. However, it down-regulated the expression of AQP4 in ARB2015 but had no effect on AVP expression. The expression of RNase III family enzymes also was altered by WR in a population-dependent manner, with DICER1 being down-regulated in JF and RB1995, Drosha was decreased in RB1995, and ARG2 was up-regulated in ARB2015. The expression of DGCR8 and TRBP1 was not affected by WR in any population; however, DGCR8 mRNA levels were significantly lower in RB1995 and ARB2015 compared to JF under both conditions. TRBP1 gene expression was significantly lower in RB1995 and ARB2015 compared to JF under WR conditions. In the blood, the expression of these genes also was altered by WR, but with different patterns than the kidney. The mRNA abundances of AQP, AVP, DICER1, DGCR8, AGO2, and TRBP1 were significantly decreased by WR in RB1995. However, the expression of AQP2, AVP, DGCR8, and TRBP1 was increased in WR-ARB2015 compared to the control. In the JF, there was no difference in the expression of these genes except for a significant up-regulation of TRBP1 in WR compared to the control group. To the best of our knowledge, this is the first report showing that water channels and the RNase III enzymes are differentially regulated by WR in a population-dependent manner, which may be due to differential postnatal growth and maturation. Their expression in the circulation could open new vistas for identification of new molecular signatures involved in adaptation to water-deprivation stress.