Directed migration of cells toward chemokines underpins a multitude of processes required for the initiation, differentiation and effector phases of adaptive immune responses. In skin, a rising immobilized gradient of lymphatic endothelial cell-derived CCL21 guides CCR7-dependent haptotaxis of mature dendritic cells into afferent lymphatic vessels to facilitate priming of immune responses in draining lymph nodes. The immobilized dermal CCL21 gradient permits efficient dendritic cell homing, however the molecular mechanisms that maintain this gradient in vivo are not well understood. Here we identify an important role for the atypical chemokine receptor 4 (ACKR4) in regulating abundance and distribution of CCR7 ligands CCL19 and CCL21 in skin. Dermal CCL19/21 regulation was dependent on ACKR4 function within radio-resistant cells, of which a subpopulation of dermal fibroblasts exhibited the greatest level of ACKR4 expression. CCL19/21 hyperabundance in the absence of ACKR4 impeded CCR7-dependent homing of dermal dendritic cells into lymphatic vessels and subsequent accumulation in draining lymph nodes. Strikingly, dermal ACKR4 also limited leaching and accrual of peripheral chemokines in draining lymph nodes, independent of ACKR4-scavenging activity in subcapsular sinus ceiling lymphatic endothelial cells. These findings identify an important physiological role for dermal ACKR4-mediated chemokine sequestration in regulating haptotactic chemokine gradients vital for the activation of the adaptive immune system, and also indicate that dermal ACKR4 limits chemokine dissemination and accumulation at distal sites.