"I do believe that he messed up in his comments on Tuesday when it sounded like a moral equivocation or at the very least moral ambiguity when we need extreme moral clarity," Ryan told CNN's Jake Tapper at a town hall in Racine, Wisconsin,
referencing a news conference Trump had last week.
The Wisconsin Republican's criticism of the President was clear and unsparing even as Ryan said that he believes the President has since clarified his comments.
It's not the first time Ryan has criticized Trump's rhetoric, but his break with Trump was significant as the speaker prepares to work with the President on a full agenda this fall including tax reform and raising the debt ceiling.
When asked by an audience member whether he would back censuring Trump, Ryan said he would not back such a measure, adding that the issue cannot devolve into a partisan fight.
Throughout the town hall Monday, Ryan was asked about Trump's behavior and how he handles the President's tweeting and his comments.
Ryan said that he tries to lead by example, but that ultimately he just wants Trump to succeed.
"Do I wish there would be a little less tweeting? Of course I do," he said.
Ryan, however, did praise the President's plans on Afghanistan and said he was especially happy with how Trump came to his decision.
"I'm pleased with the decision," Ryan said just minutes after Trump finished his speech at Fort Myer in Arlington, Virginia.
"We cannot allow another safe haven for terrorists to materialize again."
Ryan added that he believed he'd heard "principled realism" and a new "doctrine" Monday night from Trump.
But Afghanistan was just one of the foreign conflicts Ryan weighed in on.
Asked whether Trump's rhetoric on North Korea has been too aggressive, Ryan said that North Korea is a "serious threat."
"I think it is important that (Kim Jong Un) realizes we aren't going to take things lying down," Ryan said.
On the domestic front, Ryan has a full agenda ahead when he returns in September on top of one piece of unfinished business that eluded the Republican-controlled Congress this summer.
While the House of Representatives voted to repeal and replace the Affordable Care Act, Ryan used the town hall Monday to encourage the Senate -- where the bill failed by a single vote -- to get back to work.
"The House has passed its bill. We're waiting for the Senate to pass theirs," Ryan said. "Doing nothing really isn't an option."
One constituent expressed frustration with how Republicans had failed to make good on their seven-year campaign promise to gut Obamacare. Another one asked point blank how Ryan planned to make sure that tax reform didn't meet the same fate as the GOP's health care effort.
But there are other tasks that Congress has to do this fall on top of the ones Republicans want to do.
House Republicans also have yet to pass a budget due to infighting within their conference. And when they return, Republicans will need to move to fund the government and raise the country's debt ceiling.
Monday's town hall was the first town hall meeting Ryan has held in his home district in nearly two years, the Milwaukee Journal Sentinel reported
, a point his critics have used to hammer the Wisconsin Republican.
In response to questions about when his last town hall was in his district, a spokesperson emphasized Ryan's other outreach to constituents including a CNN town hall that Ryan held in Washington earlier this year, as well as business town halls and telephone town halls.
This story has been updated and will update with additional news.