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Flaxseed (Linum usitatissimum L.) mucilage is one of the most studied plant seed gums in terms of its techno-functional and health-promoting properties. Nonetheless, the interplay of flaxseed gum (FG) with other food biopolymers, such as milk proteins, under in vitro digestion conditions remains underexplored. The aim of the present work was to investigate the colloidal interplay between flaxseed gum (golden or brown) and milk proteins (sodium caseinate or whey protein isolate) under simulated in vitro digestion conditions and its relationship with the attained in vitro protein digestibility. The presence of flaxseed gum in the milk protein food models and in the oral food boluses obtained was associated with the occurrence of segregative microphase separation. Flaxseed gum exhibited a prominent role in controlling the acid-mediated protein aggregation phenomena, particularly in the sodium caseinate gastric chymes. The addition of FG in the food models was associated with a higher amount of intact total caseins and β-lactoglobulin at the end of the gastric processing step. Monitoring of the intestinal processing step revealed a very advanced cleavage of the whey proteins (>98%) and caseins (>90%). The degree of the milk protein hydrolysis achieved at the end of the intestinal processing was significantly higher in the systems containing flaxseed gum (i.e., 59–62%) than their gum-free protein counterparts (i.e., 46–47%). It was postulated that the electrostatic milk protein complexation capacity and, to a lesser extent, the thickening effect of flaxseed gum influenced the in vitro digestibility of the milk proteins.