Dogs and cats make short-term food choices based on palatability. We hypothesized that, if palatability were masked, long-term food choices would be based on physiological requirements, and circulating metabolite concentrations would reflect those choices. Four experimental foods with similar palatability, but varying in macronutrient composition, were prepared for healthy adult dogs (=17) and cats (=27). Food 1 was high protein; food 2 was high fat; food 3 was high carbohydrates; and food 4 was balanced for macronutrients. By choosing any combination of foods, dogs and cats could individually set their macronutrient intake. Plasma metabolomic profiles were determined at baseline and after animals had consumed their food intake of choice for 28 days. Based on food intake calculations over 28 days, dogs on average chose to consume most of their calories from fat (41.1±4.3%) and then carbohydrate (35.8±3.7%), whereas cats on average chose to consume most of their calories from carbohydrate (43.1±4.0%) and then protein (30.3±3.9%; all <0.001). Age and lean or fat body mass also influenced protein intake. Younger, leaner cats consumed more protein compared with older cats, whereas younger, leaner dogs consumed less protein compared with dogs having more fat body mass. Older cats with moderate protein intake had lower circulating docosahexaenoic acid (DHA) concentrations as well as higher concentrations of sulfated microbial catabolic products compared with younger, leaner cats. In summary, when fed foods with similar palatability, dogs and cats consume different macronutrient compositions, and concentrations of circulating metabolites in cats reflect food choices.