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Cardiovascular reactions to psychological stressors are associated with cardiovascular disease (CVD) risk. Human brain imaging studies have identified brain regions and systems implicated in generating and regulating stressor-evoked cardiovascular reactivity, yet the reliability and generalizability of these findings remain unclear. Predictive modeling using multivariate and machine learning approaches has the promise of developing signatures of brain activity that can reliably predict outcomes, yet few studies have applied these approaches toward identifying signatures of stressor-evoked cardiovascular reactivity. Thus, the aims of the present study were (1) to develop novel multivariate signatures of stressor-evoked brain activity that could reliably predict concurrent cardiovascular physiology during stress within individuals, and (2) to evaluate whether previously reported brain signatures of cardiovascular reactivity generalize to new individuals, stressor contexts, and measures of cardiovascular physiology. Participants were 242 midlife adults (118 men and 124 women; age 30 to 51 years; 71% white) without psychiatric, immune, or cardiovascular diagnoses. Participants completed two validated cognitive stressor tasks during functional magnetic resonance imaging (fMRI) and concurrent monitoring of systolic blood pressure (SBP) and heart rate (HR). Multivariate machine learning models combining dimensionality reduction, regularized regression, and cross-validation were used to predict within-participant changes in SBP and HR during stress. Separately, two previously published multivariate signatures were applied to maps of stressor-evoked brain activity to predict SBP and HR. Contrary to hypotheses and prior reports, multivariate patterns of stressor-evoked brain activity did not reliably predict changes in SBP and HR during stress. Notwithstanding their unreliable prediction of SBP and HR, brain activity patterns relating to SBP and HR were comprised of brain regions implicated in psychological stress and physiological control processes. In addition, two previously published multivariate brain signatures of stressor-evoked cardiovascular reactivity were found to modestly predict changes in SBP and HR during stress. These findings extend our understanding of the reliability and stability of fMRI-based signatures reflecting brain processes that may link stressful experiences to CVD risk.