We have previously demonstrated that increasing the habitual protein intake widened the gap in nutritional quality between proteins through mechanisms that are not yet fully understood. We hypothesized that the differences in gastrointestinal kinetics between dietary proteins were an important factor affecting their differential response to an increased protein intake. To test this hypothesis, we built a 13-compartment model providing integrative insight into the sequential dynamics of meal nitrogen (Nm) absorption, splanchnic uptake, and metabolism, and subsequent peripheral transfer and deposition. The model was developed from data on postprandial Nm kinetics in certain accessible pools, obtained from subjects having ingested a 15 N-labeled milk or soy protein meal, after adaptation to normal (NP) or high (HP) protein diets. The faster absorption of Nm after soy vs. milk caused its earlier and stronger splanchnic delivery, which favored its local catabolic utilization (up to +30%) and limited its peripheral accretion (down to −20%). Nm absorption was also accelerated after HP vs. NP adaptation, and this kinetic effect accounted for most of the HP-induced increase (up to +20%) in splanchnic Nm catabolic use, and the decrease (down to −25%) in peripheral Nm anabolic utilization. The HP-induced acceleration in Nm absorption was more pronounced with soy than with milk, as were the HP effects on Nm regional metabolism. Our integrative approach identified Nm absorption kinetics, which exert a direct and lasting impact on Nm splanchnic catabolic use and peripheral delivery, as being critical in adaptation to both qualitative and quantitative changes in protein intake.