Functional magnetic resonance imaging (fMRI) often relies on a hemodynamic response function (HRF), the stereotypical blood oxygen level dependent (BOLD) response elicited by a brief (<4s) stimulus. Early measurements of the HRF used coarse spatial resolutions (≥3mm voxels) that would generally include contributions from white matter, gray matter, and the extra-pial compartment (the space between the pial surface and skull including pial blood vessels) within each voxel. To resolve these contributions, high-resolution fMRI (0.9-mm voxels) was performed at 3T in early visual cortex and its apposed white-matter and extra-pial compartments. The results characterized the depth dependence of the HRF and its reliability during nine fMRI sessions. Significant HRFs were observed in white-matter and extra-pial compartments as well as in gray matter. White-matter HRFs were faster and weaker than in the gray matter, while extra-pial HRFs were comparatively slower and stronger. Depth trends of the HRF peak amplitude were stable throughout a broad depth range that included all three compartments for each session. Across sessions, however, the depth trend of HRF peak amplitudes was stable only in the white matter and deep-intermediate gray matter, while there were strong session-to-session variations in the superficial gray matter and the extra-pial compartment. Thus, high-resolution fMRI can resolve significant and dynamically distinct HRFs in gray matter, white matter, and extra-pial compartments.