Molecular evolutionary rate heterogeneity—the violation of a molecular clock—is a prominent feature of many phylogenetic datasets. It has particular importance to systematists not only because of its biological implications, but also for its practical effects on our ability to infer and date evolutionary events. Here we show, using both maximum likelihood and Bayesian approaches, that a remarkably strong increase in substitution rate in the vittarioid ferns is consistent across the nuclear and plastid genomes. Contrary to some expectations, this rate increase is not due to selective forces; the vittarioids bear no signature of the change in the relative strengths of selection and drift that one would expect if the rate increase was caused by altered fixation rates. Instead, the substitution rate increase appears to stem from an elevated supply of mutations, perhaps limited to the vittarioid ancestral branch. This generalized rate increase is accompanied by extensive fine-scale heterogeneity in rates across loci, genomes, and taxa. Our analyses demonstrate the power and flexibility of trait-free investigations of rate heterogeneity within a model selection framework, emphasize the importance of explicit tests for signatures of selection prior to invoking selection-related or demography-based explanations for patterns of rate variation, and illustrate some unexpected nuances in the behavior of relaxed clock methods for modeling rate heterogeneity, with implications for our ability to confidently date divergence events. In addition, our data provide strong support for the monophylly of Adiantum, and for the position of Calciphilopteris in the cheilanthoid ferns, two relationships for which convincing support was previously lacking.