Determining the timescale of virus evolution is key to understand their origin, emergence and spread. To this end, phylogenetic methods use molecular sequence data and the sampling time of virus sequences to estimate their rate of evolution and their time of origin. The evolutionary time scale of the evolution of flaviviruses has attracted considerable attention due to the propensity of these viruses to cause human disease and their broad host range. For example, phylogenetic methods have been used to challenge the notion that slave trade was the sole factor responsible for the spread of yellow fever, and other human disease flaviviruses, to the New World. These methods have also been used to infer the mode of global dispersal of tick-borne flaviviruses. However, estimating the long-term evolutionary time scale of these viruses is much more challenging; estimates of the origin of the Flavivirus genus range from 20,000 to 300,000 years before present. These discrepancies stem from the fact that evolutionary models used in phylogenetic analyses make critical assumptions about the substitution process. Verifying the extent to which molecular data violate the model’s assumptions can be done using model adequacy methods. This is often neglected in phylogenetic analyses, misleading the resulting inferences. We present a suite of model adequacy methods for different types of molecular data and apply them to a range of flaviviruses. These methods reveal that only data sets for recently-emerging viruses satisfy the assumptions of commonly used evolutionary models. We also illustrate the extent of the bias in the estimates of evolutionary timescales via simulations. Our results suggest that the long-term evolutionary time scale of the Flavivirus genus cannot be estimated using the most commonly used methods. In this respect, wider adoption of model adequacy methods is important to avoid misleading inferences in future studies of virus evolution.