Background <p>Diagnostic classification criteria of canine meningioma remain poorly codified and have not been linked to outcome data in large scale studies employing standardized review of slides by a board of multiple pathologists.</p> Methods <p>The National Cancer Institute-led multidisciplinary Comparative Brain Tumor Consortium (CBTC) convened a meningioma pathology board, comprising both veterinarian pathologists and physician neuropathologists, and conducted a comprehensive review of 190 cases of canine meningioma. Comparative histologic and cellular features were assessed and discussed by the board for their similarities and differences to human meningioma. All cases were morphologically classified by histologic subtypes defined by the 2016 World Health Organization (WHO) and by histologic grading system for human meningioma.</p> Results <p>The majority of canine meningiomas were classified as meningothelial (140/190); most cases (109/190) were diagnosed as grade 2, 79 as grade 1, and two cases as grade 3. The histologic features with the highest agreement between reviewers were necrosis and central nervous system (CNS) invasion (intraclass correlation (ICC) of 0.44 for both features). Although morphologic features of the human grading scheme could be applied to canine tumors, there was no statistically significant difference in outcomes between grade 1 and grade 2 tumors in our patient subset with either detailed progression and cause of death information (<i>n</i> = 37) or data restricted to live/dead status (<i>n</i> = 84).</p> Conclusions <p>While similarities exist between human and canine meningioma, a revised grading framework must be utilized for canine cases, distinct from the World Health Organization classification scheme for humans. Additional studies evaluating larger numbers of similarly treated dogs are necessary, and a framework for studies to enable future meta-analysis is suggested.</p>