The fin-to-limb transition was marked by the origin of digits and the loss of dermal fin rays. Paleontological research into this transformation has focused on the evolution of the endoskeleton with little attention paid to fin ray structure and function. To address this knowledge gap, we study the dermal rays of the pectoral fins of three key tetrapodomorph taxa—Sauripterus taylori (Rhizodontida), Eusthenopteron foordi (Tristichopteridae), and Tiktaalik roseae (Elpistostegalia)—using computed tomography. These data show several trends in the lineage leading to digited forms, including the consolidation of fin rays (e.g., reduced segmentation and branching), reduction of the fin web and, unexpectedly, the evolution of asymmetry between dorsal and ventral hemitrichia. In Eusthenopteron, dorsal rays cover the preaxial endoskeleton slightly more than ventral rays. In Tiktaalik, dorsal rays fully cover the third and fourth mesomeres, while ventral rays are restricted distal to these elements, suggesting the presence of ventralized musculature at the fin tip, analogous to a fleshy ‘palm.’ Asymmetry is also observed in cross sectional area of dorsal and ventral rays. Eusthenopteron dorsal rays are slightly larger than ventral rays; by contrast, Tiktaalik dorsal rays can be several times larger than ventral rays, and degree of asymmetry appears to be greater at larger sizes. Analysis of extant osteichthyans suggests cross sectional asymmetry in the dermal rays of paired fins are plesiomorphic to crown-group osteichthyans. The evolution of dermal rays in crownward stem tetrapods reflects adaptation for a fin-supported elevated posture and resistance to substrate-based loading prior to the origin of digits.