The Ancestral Rocky Mountains system consists of a series of basement-cored uplifts and associated sedimentary basins that formed in southwestern Laurentia during Early Pennsylvanian–middle Permian time. This system was originally recognized by aprons of coarse, arkosic sandstone and conglomerate within the Paradox, Eagle, and Denver Basins, which surround the Front Range and Uncompahgre basement uplifts. However, substantial portions of Ancestral Rocky Mountain–adjacent basins are filled with carbonate or fine-grained quartzose material that is distinct from proximal arkosic rocks, and detrital zircon data from basins adjacent to the Ancestral Rocky Mountains have been interpreted to indicate that a substantial proportion of their clastic sediment was sourced from the Appalachian and/or Arctic orogenic belts and transported over long distances across Laurentia into Ancestral Rocky Mountain basins. In this study, we present new U-Pb detrital zircon data from 72 samples from strata within the Denver Basin, Eagle Basin, Paradox Basin, northern Arizona shelf, Pedregosa Basin, and Keeler–Lone Pine Basin spanning ∼50 m.y. and compare these to published data from 241 samples from across Laurentia. Traditional visual comparison and inverse modeling methods map sediment transport pathways within the Ancestral Rocky Mountains system and indicate that proximal basins were filled with detritus eroded from nearby basement uplifts, whereas distal portions of these basins were filled with a mix of local sediment and sediment derived from marginal Laurentian sources including the Arctic Ellesmerian orogen and possibly the northern Appalachian orogen. This sediment was transported to southwestern Laurentia via a ca. 2,000-km-long longshore and aeolian system analogous to the modern Namibian coast. Deformation of the Ancestral Rocky Mountains slowed in Permian time, reducing basinal accommodation and allowing marginal clastic sources to overwhelm the system.