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Arginine vasopressin (Avp) is a conserved pleiotropic hormone that is known to regulate both water reabsorption and ion balance; however, many of the mechanisms underlying its effects remain unclear. Here, we used zebrafish embryos to investigate how Avp modulates ion and acid–base homeostasis. After incubating embryos in double-deionized water for 24 h, <i>avp</i> mRNA expression levels were significantly upregulated. Knockdown of Avp protein expression by an antisense morpholino oligonucleotide (MO) reduced the expression of ionocyte-related genes and downregulated whole-body Cl⁻ content and H⁺ secretion, while Na⁺ and Ca²⁺ levels were not affected. Incubation of Avp antagonist SR49059 also downregulated the mRNA expression of sodium chloride cotransporter 2b (<i>ncc2b</i>), which is a transporter responsible for Cl⁻ uptake. Correspondingly, <i>avp</i> morphants showed lower NCC and H⁺-ATPase rich (HR) cell numbers, but Na⁺/K⁺-ATPase rich (NaR) cell numbers remained unchanged. <i>avp</i> MO also downregulated the numbers of <i>foxi3a</i>- and p63-expressing cells. Finally, the mRNA expression levels of <i>calcitonin gene-related peptide</i> (<i>cgrp</i>) and its receptor, <i>calcitonin receptor-like 1</i> (<i>crlr1</i>), were downregulated in <i>avp</i> morphants, suggesting that Avp might affect Cgrp and Crlr1 for modulating Cl⁻ balance. Together, our results reveal a molecular/cellular pathway through which Avp regulates ion and acid–base balance, providing new insights into its function.