In the Pucciniomycetes, a class of fungi that includes the plant pathogenic rust fungi, insect parasitism is restricted to a single family, the Septobasidiaceae. The Septobasidiaceae form a variety of symbioses with scale insects and have remained largely unstudied since the 1930s. Transitions between plant and animal parasitism and between mutualism and parasitism cannot be fully addressed in the Basidiomycota without a clear phylogenetic hypothesis for the Septobasidiales. Here, molecular phylogenetic methods were applied to understand the origin of scale insect parasitism, test the monophyly of the order Septobasidiales, and evaluate the infrageneric concepts in the largest genus of scale insect parasites, Septobasidium. DNA sequence data from rRNA genes were used to infer higher-level relationships within the Pucciniomycetes, and data from translation elongation factor 1-alpha (tef1) were added for phylogenetic inference within the Septobasidiaceae. Data from tef1 revealed different intron arrangements within Septobasidium, but the molecule did not provide much additional phylogenetically informative data. Likelihood-model-based phylogenetic analyses of 44 Pucciniomycotina taxa provided moderate support for a single origin of insect parasitism. Within the Septobasidiaceae, there was little or no support for a monophyletic Septobasidium, and well-resolved subclades of Septobasidium species contradict previous morphological delimitations of groups within the genus.