Kyiv appeared to be one of the main targets of the attack. The thuds of air defense batteries and the staccato bursts of heavy machine guns echoed through the night in the capital, as military units defending the city tried to take down missiles streaking overhead and attack drones that swooped in, their ominous buzz trailing over neighborhoods.

Multiple fires were reported across Kyiv, including at a 16-story apartment block. Another fire near the city center covered an area of more than 5,000 square feet. Of the four people who died in Kyiv, three were rescuers who had rushed to extinguish the fires, Ukrainian authorities said. Kyiv’s mayor, Vitali Klitschko, also said that 20 people had been injured in the capital, and that search-and-rescue operations were ongoing in several locations.

The Ukrainian Air Force reported that Russia had launched ballistic missiles, cruise missiles and drones at other cities across Ukraine, including Odesa in the south and Ternopil in the west. The extent of the damage and casualties outside Kyiv was not immediately clear.

The attack Friday was part of a broader Russian campaign to bombard Ukrainian cities with swarms of drones and missiles in recent weeks, combined with a renewed ground offensive in the east. Russia has launched more than 1,000 drones per week at military and civilian targets in Ukraine in recent months, including nearly 500 in a single night last week.

The attack also came shortly after President Vladimir V. Putin warned President Trump on Wednesday that Russia would retaliate for Ukraine’s strikes on its bombers last weekend, further dimming hopes for a cease-fire that were already faint.

The Ukrainian attack, which involved smuggling drones deep into the Russian heartland and launching them from semi trucks, destroyed or damaged at least a dozen aircraft, including many of Moscow’s nuclear-capable strategic bombers.

It was one of the war’s most audacious strikes, exposing Russian vulnerabilities, delivering a humiliating blow to the country’s military, and signaling to the world, including President Trump, that Ukraine still holds cards in the fight.

“They attacked pretty harshly. They went deep into Russia,” Mr. Trump said on Thursday about the Ukrainian assault. He noted that Mr. Putin, during their call, had told him Russia had “no choice” but to retaliate. “And it’s probably not going to be pretty,” Mr. Trump added.

Mr. Trump also compared Russia and Ukraine to two fighting children who needed to work out their differences before their bloody war could end.

“Sometimes you’re better off letting them fight for a while and then pulling them apart,” he said in the Oval Office as Germany’s chancellor, Friedrich Merz, urged him to leverage the power of the United States to end the conflict.

Mr. Trump avoided answering a question about whether he was willing to increase pressure on Russia. The Kremlin has repeatedly resisted his calls for an unconditional cease-fire.

Since the beginning of this year, the Russian military has carried out attacks against Ukraine using nearly 27,700 aerial bombs, almost 11,200 Shahed drones, around 9,000 other attack strike drones and more than 700 missiles, including ballistic ones, President Volodymyr Zelensky of Ukraine said on Thursday.

“This is the pace of Russian strikes, and they deliberately set this tempo from the very first days of the full-scale war,” Mr. Zelensky said. “Russia has restructured its entire state, society, and economy to be able to kill people in other countries on a massive scale and with impunity.”

Before the overnight bombardment, Russia launched high-explosive aerial bombs at the center of the southern Ukrainian city of Kherson on Thursday morning, partially destroying the Regional State Administration building and damaging several surrounding structures.

On Wednesday night, the Russians attacked the city of Pryluky in the northeastern Chernihiv region, killing at least five people, including a 1-year-old baby, Ukrainian officials said.