The ventromedial prefrontal cortex (vmPFC) integrates sensory, affective, memory‐related, and social information from diverse brain systems to coordinate behavioral and peripheral physiological responses according to contextual demands that are appraised as stressful. However, the functionality of the vmPFC during stressful experiences is not fully understood. Among 40 female participants, the present study evaluated (a) functional connectivity of the vmPFC during exposure to and recovery following an acute psychological stressor, (b) associations among vmPFC functional connectivity, heart rate, and subjective reports of stress across individuals, and (c) whether patterns of vmPFC functional connectivity were associated with distributed brain networks. Results showed that psychological stress increased vmPFC functional connectivity with individual brain areas implicated in stressor processing (e.g., insula, amygdala, anterior cingulate cortex) and decreased connectivity with the posterior cingulate cortex and thalamus. There were no statistical differences in vmPFC connectivity to individual brain areas during recovery, as compared with baseline. Spatial similarity analyses revealed stressor‐evoked increased connectivity of the vmPFC with the so‐called dorsal attention, ventral attention, and frontoparietal networks, as well as decreased connectivity with the default mode network. During recovery, vmPFC connectivity increased with the frontoparietal network. Finally, individual differences in heart rate and perceived stress were associated with vmPFC connectivity to the ventral attention, frontoparietal, and default mode networks. Psychological stress appears to alter network‐level functional connectivity of the vmPFC in a manner that further relates to individual differences in stressor‐evoked cardiovascular and affective reactivity.