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In the present study, we aimed at assessing the influence of breed and feeding system on the bovine milk profile of betaines and carnitines and milk capacity in counteracting the inflammatory endothelial cell (EC) damage induced by interleukin (IL)-6. In the first experimental design, two breeds were chosen (<i>Holstein</i> vs. <i>Modicana</i>) to investigate the biomolecule content and antioxidant capacity in milk and dairy products. In the second experimental design, two feeding systems (pasture vs. total mixed ratio) were tested only in <i>Holstein</i> to evaluate the possible effect on the functional profile of milk and dairy products. Finally, the bulk milk from the two experimental designs was used to evaluate the efficacy of preventing IL-6-induced endothelial inflammatory damage. Results showed that <i>Modicana</i> milk and whey had higher biomolecule content and antioxidant activity compared to <i>Holstein</i> milk (<i>p</i> < 0.01). Milk from <i>Holstein</i> fed TMR showed higher concentration of γ-butyrobetaine, δ-valerobetaine (<i>p</i> < 0.01), and <span style="font-variant: small-caps;">l</span>-carnitine (<i>p</i> < 0.05). Similarly, whey from <i>Holstein</i> fed TMR also showed higher content of δ-valerobetaine, glycine betaine, <span style="font-variant: small-caps;">l</span>-carnitine, and acetyl-<span style="font-variant: small-caps;">l</span>-carnitine (<i>p</i> < 0.01) compared to the <i>Holstein</i> fed pasture. Conversely, the antioxidant activity of milk and dairy products was not affected by the feeding system. In ECs, all milk samples reduced the IL-6-induced cytokine release, as well as the accumulation of reactive oxygen species (ROS) and the induction of cell death, with the most robust effect elicited by <i>Modicana</i> milk (<i>p</i> < 0.01). Overall, <i>Modicana</i> milk showed a higher content of biomolecules and antioxidant activity compared to <i>Holstein</i>, suggesting that the breed, more than the feeding system, can positively affect the health-promoting profile of dairy cattle milk.