The ileum is considered the primary site of inorganic sulfate (SO₄^2-) absorption. In the present study, we explored the contributions of the apical chloride/bicarbonate (Cl^-/HCO₃^-) exchangers DRA (Slc26a3), and PAT1 (Slc26a6), to the underlying transport mechanism. Transepithelial ³⁵SO₄^2- and ³⁶Cl^- fluxes were determined across isolated, short-circuited segments of the distal ileum from wild-type (WT), DRA-knockout (KO) and PAT1-KO mice, together with measurements of urine and plasma sulfate. The WT distal ileum supported net sulfate absorption (197.37 ± 13.61 nmol/cm²/h), but neither DRA nor PAT1 directly contributed to the unidirectional mucosal-to-serosal flux (J_ms^SO4), which was sensitive to serosal (but not mucosal) DIDS, dependent on Cl^-, and regulated by cAMP. However, the absence of DRA significantly enhanced net sulfate absorption by one-third via a simultaneous rise in J_ms^SO4 and a 30 % reduction to the secretory s-to-m flux (J_sm^SO4). We propose that DRA, together with PAT1, contribute to J_sm^SO4 by mediating sulfate efflux across the apical membrane. Associated with increased ileal sulfate absorption in vitro, plasma sulfate was 61 % greater, and urinary sulfate excretion (U_SO4) 2.2-fold higher, in DRA-KO mice compared to WT controls, while U_SO4 was increased 1.8-fold in PAT1-KO mice. These alterations to sulfate homeostasis could not be accounted for by any changes to renal sulfate handling suggesting the source of this additional sulfate was intestinal. In summary, we characterized transepithelial sulfate fluxes across the mouse distal ileum demonstrating that DRA (and to a lesser extent, PAT1), secrete sulfate with significant implications for intestinal sulfate absorption and overall homeostasis.