Studies employing functional connectivity-type analyses have established that spontaneous fluctuations in functional magnetic resonance imaging (fMRI) signals are organized within large-scale brain networks. Meanwhile, fMRI signals have been shown to exhibit 1/f-type power spectra — a hallmark of scale-free dynamics. We studied the interplay between functional connectivity and scale-free dynamics in fMRI signals, utilizing the fractal connectivity framework — a multivariate extension of the univariate fractional Gaussian noise model, which relies on a wavelet formulation for robust parameter estimation. We applied this framework to fMRI data acquired from healthy young adults at rest and while performing a visual detection task. First, we found that scale-invariance existed beyond univariate dynamics, being present also in bivariate cross-temporal dynamics. Second, we observed that frequencies within the scale-free range do not contribute evenly to inter-regional connectivity, with a systematically stronger contribution of the lowest frequencies, both at rest and during task. Third, in addition to a decrease of the Hurst exponent and inter-regional correlations, task performance modified cross-temporal dynamics, inducing a larger contribution of the highest frequencies within the scale-free range to global correlation. Lastly, we found that across individuals, a weaker task modulation of the frequency contribution to inter-regional connectivity was associated with better task performance manifesting as shorter and less variable reaction times. These findings bring together two related fields that have hitherto been studied separately — resting-state networks and scale-free dynamics, and show that scale-free dynamics of human brain activity manifest in cross-regional interactions as well.