Infusion of l-arginine produces an increase in glomerular filtration via kidney vasodilation, correlating with increased kidney excretion of nitric oxide (NO) metabolites, but the specific underlying mechanisms are unknown. We utilized clearance and micropuncture techniques to examine the whole kidney GFR and single nephron GFR (SNGFR) responses to 1) l-arginine (ARG) 2) ARG + octreotide (OCT) to block insulin release, 3) ARG + OCT + insulin (INS) infusion to duplicate ARG induced insulin levels and 4) Losartan (LOS), an angiotensin AT-1 receptor blocker, + ARG + OCT. ARG infusion increased GFR, while increasing insulin levels. OCT co-infusion prevented this increase, but with insulin infusion to duplicate ARG induced rise in insulin, the GFR response was restored. Identical insulin levels in the absence of ARG had no effect on GFR. In contrast to ARG infusion alone, co-infusion of OCT with ARG reduced proximal tubular fractional and absolute reabsorption potentially activating tubuloglomerular feedback. Losartan infusion, in addition to ARG and OCT (LOS+ARG+OCT), restored the increase in both SNGFR and proximal tubular reabsorption, without increasing insulin levels. In conclusion, 1) Hyperfiltration responses to ARG require the concurrent, modest, permissive increase in insulin 2) Inhibition of insulin release after ARG reduces proximal reabsorption and prevents the hyperfiltration response. 3) Inhibition of angiotensin II (Ang II) activity restores and, in fact, magnifies the hyperfiltration response, maintains parallel increases in proximal reabsorption and overrides the arginine/octreotide actions.