Carotenoid-based colors serve important sexual-signaling functions in many animals, but the proximate factor(s) underlying their expression has sparked controversy. In particular, the relative contributions of dietary and physiological mechanisms have been questioned of late. However, no studies have concurrently quantified levels of food intake or pigment processing in any species to examine the comparative effects of pigment acquisition and use on integumetary coloration. Here, we studied within- and between-sex patterns of food intake and plasma pigment circulation in the Zebra Finch (Taeniopygia guttata) to assess how sexually dichromatic, carotenoid-based bill pigmentation serves as an indicator of pigment access in the diet and carotenoid transport through the bloodstream. First, in a food-choice study, we found that males and females did not consume different types or amounts of food, despite dramatic sex differences in bill coloration. Similarly, variability in carotenoid-based bill pigmentation within each sex was uncoupled from levels of food consumption. Next, we used high-performance liquid-chromatography (HPLC) to quantify the types and amounts of carotenoids circulating through blood. Male and female Zebra Finches circulated the same four major carotenoid pigments in blood plasma (lutein, zeaxanthin, anhydrolutein, and β-cryptoxanthin), but males circulated a significantly higher concentration of plasma carotenoids than did females. Within both sexes, individuals that circulated more carotenoid pigments displayed more brightly colored bills. In sum, these results suggest that physiological factors such as pigment transport may play a more important role in shaping variability in carotenoid-based bill coloration in this species than does diet. Future studies should be aimed at identifying the proximate determinants of plasma carotenoid circulation in these birds as well as how circulated pigments are used to produce maximum color displays.