The Erythropeltidales are a common group of small, mostly epiphytic, marine red algae. Morphologically, they can be divided into two main groups: species that are crustose and species that are upright. Being morphologically simple, generic boundaries and evolutionary trends are controversial or unknown. We focus our molecular phylogenetic analysis on members that are crustose using samples collected from around the world and placed in unialgal culture. Our data indicate that one upright genus, Porphyropsis, is closely related to crustose genera and that the upright habit evolved at least twice in the order. In addition, the genus Sahlingia is supported as distinct from Erythrocladia. Within samples identified as Erythrocladia, three groups are distinguished: Erythrocladia, composed of crustose aggregating filaments with pyrenoids; Pseudoerythrocladia gen. nov., crustose aggregating filaments without pyrenoids, a sister genus to Porphyropsis also without pyrenoids; and Madagascaria gen. nov., a sister genus to all other Erythropeltidales samples that is only subtly different from Erythrocladia. Within these genera, no clear morphological groups are evident, nor is the level of molecular diversity suggestive of multiple species. We suggest that described species, especially in the genus Erythrocladia, are just morphological variants, due to substrate or environmental variation, and further descriptions of these morphologically simple algae must incorporate molecular data and standardized culture conditions.