RAG endonuclease initiates Igh V(D)J recombination in progenitor B cells by binding a J-recombination signal sequence (RSS) within a recombination centre (RC) and then linearly scanning upstream chromatin, presented by loop extrusion mediated by cohesin, for convergent D-RSSs. The utilization of convergently oriented RSSs and cryptic RSSs is intrinsic to long-range RAG scanning. Scanning of RAG from the DJ-RC-RSS to upstream convergent V-RSSs is impeded by D-proximal CTCF-binding elements (CBEs). Primary progenitor B cells undergo a mechanistically undefined contraction of the V locus that is proposed to provide distal Vs access to the DJ-RC. Here we report that an inversion of the entire 2.4-Mb V locus in mouse primary progenitor B cells abrogates rearrangement of both V-RSSs and normally convergent cryptic RSSs, even though locus contraction still occurs. In addition, this inversion activated both the utilization of cryptic V-RSSs that are normally in opposite orientation and RAG scanning beyond the V locus through several convergent CBE domains to the telomere. Together, these findings imply that broad deregulation of CBE impediments in primary progenitor B cells promotes RAG scanning of the V locus mediated by loop extrusion. We further found that the expression of wings apart-like protein homologue (WAPL), a cohesin-unloading factor, was low in primary progenitor B cells compared with v-Abl-transformed progenitor B cell lines that lacked contraction and RAG scanning of the V locus. Correspondingly, depletion of WAPL in v-Abl-transformed lines activated both processes, further implicating loop extrusion in the locus contraction mechanism.