Headed by Fiona Davies, a former recruitment sales director at Trinity Mirror's Hot Group, the team aims to improve the publisher's relationship with recruitment agencies, which have not traditionally advertised in its papers.
Until now, job advertisers have been offered a package combining print and online and have had to put in a specific request if they want to opt out of either platform.
The new sales team will push an online-only option, in contrast with Northcliffe Media, which was recently criticised for forcing recruitment advertisers to pay for an additional online insertion if they wanted to place an ad in one of the group's regional papers.
Johnston's advertisers can now manage their inventories online, including CV matching, and jobseekers can do more filtered searches by salary, location and sector.
Johnston will promote the relaunch with a marketing campaign in papers published in the 20 largest towns where it operates.
Alex Green, Johnston Press' director of digital, said that 90% of the local newspaper group's online jobseekers also use print ads.
He added: "It's been a market that the local press hasn't really attracted and while the focus is initially on growing the online business, over time we will do more cross-selling."