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Western North America contains a mosaic of indigenous and introduced red fox (Vulpes vulpes) populations. Historically, native red foxes occurred in subalpine zones of the Cascade, Rocky, and Sierra Nevada mountain ranges, and in the desert-like Sacramento Valley of California. The origins of red foxes observed in the Intermountain West since the early 1900s are unclear, potentially representing native population relicts from the last ice age, dispersers from adjacent mountain populations, or early fur-farm escapees. These foxes carry a native 696-bp mitochondrial haplotype (A-19), which was also the most basal and widespread among western populations and thus equally consistent with ancient and contemporary origins. Here, to increase resolution, we sequenced an additional 3,308 bp (totaling 4,004 bp) of the mitochondrial genome corresponding to A-19 and related haplotypes (O-24 and D-19) from historical and modern samples collected throughout western North America. The expanded sequences revealed previously undocumented haplotype diversity, including another novel mutation associated with the D-19 matriline endemic to the Sacramento Valley, confirming its ancient divergence. We observed 6 A-19 variants falling into 2 divergent subclades. Although no A-19 variants were unique to the Intermountain West, the 2 dominant ones were rare elsewhere, and an analysis of molecular variance supported the distinctiveness of this population. Our findings suggest this population was either an ancient relict or derived from a small founder group from a neighboring mountain range. Additional sampling and high-density nuclear genomic markers can further clarify origins of these animals, including potential nonnative introgression.