The white-pine blister rust fungus, Cronartium ribicola Fisch. in Rabenh., continues to spread in North America, utilizing various aecial (primary) and telial (alternate) hosts, some of which have only recently been discovered. This introduced pathogen has been characterized as having low genetic diversity in North America, yet it has demonstrated a capacity to invade diverse environments. The recent discovery of this rust fungus on the telial host Pedicularis racemosa Dougl. ex Benth., raises questions of whether this host association represents a recent acquisition by C. ribicola or a long-standing host association that was overlooked. Here we explore two questions: (i) is host specialization detectable at a local scale and (ii) is the capacity to infect Pedicularis racemosa local or widespread? Genetic analysis of C. ribicola isolates from different aecial and telial hosts provided no evidence for genetic differentiation and showed similar levels of expected heterozygosity within a geographic population. An inoculation test showed that diverse C. ribicola sources from across North America had the capacity to infect Pedicularis racemosa. These results support a hypothesis that ability to infect Pedicularis racemosa is common in C. ribicola from North America. Utilization of Pedicularis racemosa by C. ribicola may be dependent on the co-occurrence of this host, inoculum, and favorable environments.