At a time when Ukraine is fighting and negotiating for its very survival, his resignation is hugely destabilising.
Talks will continue next week. Ukraine's presidential office said on Saturday that Defence Minister Rustem Umerov was the head of a delegation heading to the US.
What is not known is whether this will be a timely reboot for Kyiv, or a costly lack of continuity.
It is also not known how Yermak is taking his sudden departure from government. The New York Post reported on Saturday that he had texted their paper and vowed to go to the front line. He also declared his innocence.
"I'm going to the front and am prepared for any reprisals," he reportedly said. "I am an honest and decent person."
But there is a feeling that Yermak's departure is a sign of positive change.
"Let's call it what it is: good news," says Olga Rudenko, editor of the Kyiv Independent.
"Think about it: a young democracy like Ukraine has independent institutions that are strong enough to investigate the most powerful man in the country - and to do so during the war.
"People rooting for Ukraine around the world aren't rooting for a place on the map, but for a place living by certain values - and fighting for them. Today we see these values in action.
"This shows why Ukraine is exactly the country worth supporting."
Additional reporting by Toby Luckhurst