Pterobranchs are rare in Cambrian strata of North America despite discoveries of more than 30 exceptionally preserved fossil biotas. Miaolingian pterobranchs from this continent typically form low‐diversity and low‐abundance assemblages. Here we describe an abundant pterobranch material from the Drumian Marjum Formation recently collected at the Gray Marjum Quarry in the House Range of Utah, USA. The faunule is composed of two new species: Sphenoecium marjumensis, an encrusting representative forming compact bushy colonies of more than 80 tubes with poorly developed rhizomes, and Tarnagraptus cupidus, an erect growing taxon characterized by intertwining stems and a monopodial colonial growth. Known in extant rhabdopleurids, this mode of colonial growth had hitherto never been observed in fossil pterobranchs. Its documentation in a c. 500‐myr‐old taxon attests to its deep origin in the evolutionary history of the group. Although the new species almost exclusively occur in the Marjum strata, this pterobranch faunule is broadly similar to those recovered from other Miaolingian Burgess Shale‐type deposits of North America in terms of genus‐level composition, species richness, and ecological structure. This may indicate that pterobranchs were poorly diverse components of animal communities at that time, or that they mostly thrived in more proximal shelf environments where conditions conducive to their preservation rarely developed. The common co‐occurrence of taxa with fundamentally different ecomorphotypes in the Miaolingian Series of North America strongly suggests an earlier phase of morphological diversification of benthic pterobranchs during the early Cambrian, which remains insufficiently documented by fossils.