Tearing into "politicians who tweet and appear on cable news shows," an irate Obama said right-wing bombast and "yapping" had whipped up anger but done nothing to prevent terrorism.
The killing of 49 people at a gay nightclub in Orlando -- by a self-described Islamic State sympathizer -- has poured kerosene on already angry election-year debates over guns, terrorism, sex and faith.
The bloody attack prompted Trump to repeat his controversial proposal to ban all Muslims from entering the United States on counterterrorism grounds.
Obama took issue with Trump's plan.
"Where does this stop?" Obama demanded, shedding his usual 'no drama Obama' public persona to denounce "language that singles out immigrants and suggests entire religious communities are complicit in violence."
"Are we going to start treating all Muslim Americans differently? Are we going to start subjecting them to special surveillance? are we going to start discriminating them because of their faith?"
"We're starting to see where this kind of rhetoric and loose talk and sloppiness about who exactly we're fighting, where this can lead us."
Obama's message was echoed by his would-be heir Hillary Clinton, the presumptive Democratic nominee for president.
The two had been scheduled to campaign together on Wednesday, but the event was postponed following the Orlando shooting.
Nonetheless, they seemed to be on the same page when it came to Trump, making a concerted effort to paint him as, in Clinton's words, lacking substance, "temperamentally unfit and totally unqualified to be commander-in-chief."
"We don't need conspiracy theories and pathological self-congratulations. We need leadership, common sense, and concrete plans because we are facing a brutal enemy."
Not a strategy
Trump and his fellow Republicans regularly upbraid Obama as being weak on terror, citing his refusal to use the term "radical Islam."
"What exactly would using this label accomplish?" Obama asked.
"What exactly would it change? Would it make ISIL less committed to trying to kill Americans?" he said, using an alternate acronym for the Islamic State group. "Would it bring in more allies? Is there a military strategy that is served by this?"
"The answer is none of the above," said Obama.
"There's no magic to the phrase 'radical Islam'. It's a political talking point. It's not a strategy."
"Not once has an advisor of mine said, 'man, if we really use that phrase, we're going to turn this whole thing around.'"
Trump -- who has long fostered conspiracy theories about Obama's birthplace -- has appeared to suggest that the president may even be in league with jihadists.
"Look, we're led by a man that either is not tough, not smart or he's got something else in mind," Trump told Fox News.
"He doesn't get it or he gets it better than anybody understands -- it's one or the other, and either one is unacceptable," he added.
Obama said the idea that the administration is confused about the enemy "would come as a surprise to the thousands of terrorists who we've taken off the battlefield."
While parrying his political foes, Obama also sought to show Americans that the war against the Islamic State in Syria, Iraq and Libya, while slow, was being won.
He said the number of foreign fighters joining the extremists was plummeting.
"ISIL lost nearly half of the populated territory it had in Iraq and it will lose more. ISIL continues to lose ground in Syria as well," Obama said after a meeting of his National Security Council.
"In short, our coalition continues to be on offense. ISIL is on defense."
