Functional connectivity (FC) has shown promising utility in the field of precision psychiatry. However, to translate from research to clinical use, FC reliability and sensitivity to individual differences still require improvement. Movie watching as an acquisition state offers advantages at the whole-brain level that align with the requirements of FC for individualized measures. However, it is unclear whether these advantages hold in specific brain regions important for precision psychiatry. Here, we compared univariate and multivariate reliability-based measures of movie-watching and resting-state FC data in three psychiatrically relevant brain regions. We found that the reliability of movie-watching FC was comparable with resting-state FC in the dorsolateral prefrontal cortex and presupplementary motor area, and movie-watching FC was more discriminable than resting-state FC in the temporoparietal junction. Rest had higher reliabilities at lower data amounts (e.g., under 5 minutes of scan time). We then expanded this approach to all brain regions and showed that for image intraclass correlation coefficients (I2C2), no parcels were significantly different between movie and rest. For discriminability, 25% (94/379) of parcels were better for movie than for rest, and zero parcels were better for rest. For fingerprinting, 59 parcels were better for movie (mainly in visual and temporal regions, mean improvement in accuracy = 23%) and 4 parcels were better for rest. For researchers interested in cross-state differences in FC reliability, we provide an interactive visualization tool that displays the results for all measures and for all regions in both movie and rest. These findings suggest that movie watching as an acquisition state—even when using different movies across scans—may provide a useful alternative to resting state in research studies that require optimization of FC discriminability.