Lennartsson has previously said that it was in December 2016 that she was first was informed about the security risks involved in outsourcing the Swedish Transport Agency's IT services.
However, it has now emerged that she took part in two meetings where the Swedish Security Service, Säpo, accounted for information about the security risks. One of those meetings took place in February 2016 and the other one took place in August 2016.
On Sunday, Lennartsson told newspaper Dagens Nyheter that she had not grasped the seriousness of the situation during those meetings and does not remember the matter being mentioned there. "I made a mistake," she said.
"This means that I at least twice had the chance to ask follow-up questions, which I did not do. That mistake means that I do not think I can remain in this job," Lennartsson said.
Lennartsson's handed in her resignation at an extra government meeting called on Sunday afternoon.
Since this summer, when details of the Transport Agency IT scandal first emerged, the government has been asked several times to answer questions regarding who knew what and when.
Earlier this year, the Agency's former secretary-general stepped down over her decision to outsource IT services in a way that allowed individuals abroad, who lacked security clearance, to handle classified information.
Since then, two government ministers have resigned and the opposition is pushing for a vote of no confidence regarding the defence minister, Peter Hultqvist, who had been informed about the situation but did not pass that information on.
With the scandal now encompassing the prime minister's own state secretary, the Moderate Party's defence policy spokesperson, Hans Wallmark, told news agency TT that "an even heavier shadow falls" on Hultqvist. He said that the IT scandal is coming closer to the prime minister himself.
In addition, the leader of the opposition Centre Party, Annie Lööf, said it is important that the parliament's constitutional committee's investigation into what happened proceeds.
"The information that has emerged is very serious: that the prime minister's closest aide has known about this for a longer period. It shows a breakdown of the communication in the government offices," Lööf told TT.
On Sunday, Nils Vikmång was named as Löfven's new state secretary.