Zelensky fires his prosecutor general and intelligence chief, the top two law enforcement officials.

President Volodymyr Zelensky of Ukraine fired his country’s prosecutor general and the leader of its domestic intelligence agency on Sunday, the most significant shake-up in his government since the start of the full-scale Russian invasion in February.

The dismissals of the prosecutor general, Iryna Venediktova, and Ivan Bakanov, the leader of the Security Service of Ukraine — and a childhood friend of the president — were announced in brief decrees. In a televised speech later Sunday night, Mr. Zelensky said he was responding to a large number of treason investigations opened into employees of law enforcement agencies, including the prosecutor general’s office and the domestic security agency.

On Monday, Mr. Zelensky promoted Mr. Bakanov’s deputy, Vasyl Malyuk, as the acting head of the security service.

Mr. Zelensky’s office ordered that Ms. Venediktova, who had assumed a prominent and very public role in Ukraine’s efforts to prosecute Russian war crimes and atrocities, be removed from her position. Another decree did the same for Mr. Bakanov, citing “Article 47 of the Disciplinary Statute of the Armed Forces of Ukraine.” That pertains to “failure to perform service duties, which led to human casualties or other grave consequences.”

A total of 651 cases of high treason had been opened against law enforcement personnel, Mr. Zelensky said in his speech — and that more than 60 employees of the prosecutor’s office and the Security Service of Ukraine remained in occupied territory and were working against the state.

“Such an array of crimes against the foundations of the national security of the state and the connections detected between the employees of the security forces of Ukraine and the special services of Russia pose very serious questions to the relevant leadership,” Mr. Zelensky added.

American officials said the moves reflect Mr. Zelensky’s efforts to put more experienced leaders in key security positions.

U.S. intelligence agencies have been providing huge amounts of information to Ukrainian partners. Officials emphasized on Sunday that the firing of Mr. Bakanov was not due to any mishandling of that intelligence or any major penetration of Ukraine’s intelligence services by Russia.

The Security Service of Ukraine, known by its Ukrainian initials S.B.U., is the main domestic security and intelligence authority in Ukraine and the successor to the local branch of the Soviet-era K.G.B. With 27,000 personnel, it is Europe’s largest security agency, and faces calls for reform — by comparison, Britain’s MI5 has just 4,400 employees, according to the Atlantic Council.

While U.S. intelligence agencies have worked with the S.B.U., their main relationship during the war has been with Ukraine’s military intelligence service.

Before the invasion, most of Mr. Zelensky’s cabinet had been a revolving door. But after it, senior personnel changes had been rare — until Sunday’s firing of the two top law enforcement officials.

Mr. Zelensky’s relationship with Mr. Bakanov dates back decades. Childhood friends, the two also worked in the entertainment industry — Mr. Zelensky as an actor and Mr. Bakanov as the director of the Kvartal 95 studio.

Mr. Bakanov was one of several comedy industry veterans to follow Mr. Zelensky into government. Yet in spite of skepticism about their competence that was voiced by political opponents at home before Russia invaded Ukraine, Mr. Zelensky’s government defied expectations by maintaining operations and coordinating the country’s defense through the chaotic early months of the war.

But other officials in Mr. Zelensky’s government had blamed Mr. Bakanov for intelligence failures and for missteps that allowed the Russian army to capture the city of Kherson in the south of Ukraine with almost no fighting, and Mr. Zelensky was looking to replace him, Politico reported in June.

After Ms. Venediktova was fired on Sunday, a court ordered the country’s top anti-corruption agency, the National Anti-Corruption Bureau of Ukraine, to investigate her failure to report property on an asset and income declaration that officials are required to submit.

In addition to swiftly naming a deputy as the replacement for Mr. Bakanov, the president’s office named Oleksiy Symonenko as acting prosecutor general. Mr. Symonenko had served as Ms. Venediktova’s deputy. In 2020, he was accused by the National Anti-Corruption Bureau of Ukraine of “illegally” interfering in a corruption investigation.

Carly Olson and Julian E. Barnes contributed reporting.