Coincident with climate shifts and anthropogenic perturbations, the highly voracious jumbo squid Dosidicus gigas reached unprecedented northern latitudes along the NE Pacific margin post 1997–98. The physical or biological drivers of this expansion, as well as its ecological consequences remain unknown. Here, novel analysis from both bulk tissues and individual amino acids (Phenylalanine; Phe and Glutamic acid; Glu) in both gladii and muscle of D. gigas captured in the Northern California Current System (NCCS) documents for the first time multiple geographic origins and migration. Phe δ15N values, a proxy for habitat baseline δ15N values, confirm at least three different geographic origins that were initially detected by highly variable bulk δ15N values in gladii for squid at small sizes (<30 cm gladii length). In contrast, bulk δ15N values from gladii of large squid (>60 cm) converged, indicating feeding in a common ecosystem. The strong latitudinal gradient in Phe δ15N values from composite muscle samples further confirmed residency at a point in time for large squid in the NCCS. These results contrast with previous ideas, and indicate that small squid are highly migratory, move into the NCCS from two or more distinct geographic origins, and use this ecosystem mainly for feeding. These results represent the first direct information on the origins, immigration and habitat use of this key “invasive” predator in the NCCS, with wide implications for understanding both the mechanisms of periodic D. gigas population range expansions, and effects on ecosystem trophic structure.