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Convergent clinical and neuroimaging evidence suggests that higher vestibular function is subserved by a distributed network including visuospatial, cognitive–affective, proprioceptive, and integrative brain regions. Clinical vestibular syndromes may perturb this network, resulting in deficits across a variety of functional domains. Here, we leverage structural and functional neuroimaging to characterize this extended network in healthy control participants and patients with post‐concussive vestibular dysfunction (PCVD). Then, 27 healthy control subjects (15 females) and 18 patients with subacute PCVD (12 female) were selected for participation. Eighty‐two regions of interest (network nodes) were identified based on previous publications, group‐wise differences in BOLD signal amplitude and connectivity, and multivariate pattern analysis on affective tests. Group‐specific “core” networks, as well as a “consensus” network comprised of connections common to all participants, were then generated based on probabilistic tractography and functional connectivity between the 82 nodes and subjected to analyses of node centrality and community structure. Whereas the consensus network was comprised of affective, integrative, and vestibular nodes, PCVD participants exhibited diminished integration and centrality among vestibular and affective nodes and increased centrality of visual, supplementary motor, and frontal and cingulate eye field nodes. Clinical outcomes, derived from dynamic posturography, were associated with approximately 62% of all connections but best predicted by amygdalar, prefrontal, and cingulate connectivity. No group‐wise differences in diffusion metrics or tractography were noted. These findings indicate that cognitive, affective, and proprioceptive substrates contribute to vestibular processing and performance and highlight the need to consider these domains during clinical diagnosis and treatment planning. Convergent clinical and neuroimaging evidence suggests that higher vestibular function is subserved by a distributed network including visuospatial, cognitive–affective, proprioceptive, and integrative brain regions. In this article, we leverage structural and functional neuroimaging to characterize an extended vestibular‐cognitive network in twenty‐seven healthy control participants and eighteen patients with post‐concussive vestibular dysfunction (PCVD), determine commonalities between control and PCVD patients as a “consensus” network, and describe network differences corresponding to clinical outcomes.