Electronic pads that recognise job seekers' signatures using biometric software will be installed at centres around the UK, along with PC workstations and free wi-fi.
The computers operate on the government's network and share the same level of security against hacking and viruses.
The equipment has been tested at London Bridge Jobcentre.
"We've moved away from customers coming in and standing in a queue waiting to be directed," said Baljeet Mahal, the branch's customer services manager.
"We don't have podiums, we don't have public-access phones.
"If you look back to Job Centre Plus from years ago, we had boards with paper cards with vacancies on them - we don't have those anymore."
The Department for Work and Pensions, which runs the job centres, estimates that installing the computers will save £2m per year.
While their use will not be not monitored formally, Ms Mahal said the screens were visible and staff would "have a chat" if they saw people using them for purposes other than job hunting.
Business analyst John Oldroyd told the BBC that cyber-security was crucial for all new equipment.Job seekers can search for jobs, calculate benefits and update their CVs at the in-house computers.
"I think every organisation is a target for hackers," he said.
"Security is a high priority for every system we introduced.
"It's all protected by the Department for Work and Pensions network, there are several firewalls in place."
He added that the signature pads had been designed to store data securely.
"The signature pad is used in banks in central Europe," he said.
"It uses biometric software, which measures how somebody writes their signature.
"It's not concerned so much with the image, but the way you write it - it's very consistent and individual to you like a fingerprint."
The overall signature also has to correspond at least 80% with six sample signatures, which each individual job seeker has to provide the first time they use the device.
"In terms of the signature data we store, we don't store images, we store data which builds up a signature profile," added Mr Oldroyd.
"If anyone did hack in there's no way that could be turned back into a visible signature."