Plant-based foods contain bioactive compounds such as polyphenols that resist digestion and potentially benefit the host through interactions with their resident microbiota. Based on previous observations, we hypothesized that the probiotic Lactobacillus plantarum interacts with cranberry polyphenols and dietary oligosaccharides to synergistically impact its physiology. In this study, L. plantarum ATCC BAA-793 was grown on dietary oligosaccharides, including cranberry xyloglucans, fructooligosaccharides, and human milk oligosaccharides, in conjunction with proanthocyanidins (PACs) extracted from cranberries. As a result, L. plantarum exhibits a differential physiological response to cranberry PACs dependent on the carbohydrate source and polyphenol fraction introduced. Of the two PAC extracts evaluated, the PAC1 fraction contains higher concentrations of PACs and increased growth regardless of the oligosaccharide, whereas PAC2 positively modulates its growth during xyloglucan metabolism. Interestingly, fructooligosaccharides (FOS) are efficiently utilized in the presence of PAC1, as this L. plantarum strain does not utilize this substrate typically. Relative to glucose, oligosaccharide metabolism increases the ratio of secreted acetic acid to lactic acid. The PAC2 fraction differentially increases this ratio during cranberry xyloglucan fermentation compared with PAC1. The global transcriptome links the expression of putative polyphenol degradation genes and networks and metabolic phenotypes.