Lonnie G. Bunch III, the museum leader who opened the Smithsonian’s National Museum of African American History and Culture to critical applause and huge crowds, will serve as the next secretary of the entire Smithsonian, its most senior position.

Mr. Bunch, 66, will be the first historian and the first African-American to oversee the Smithsonian’s 19 museums and galleries, the National Zoological Park and research centers. He will take over on June 16, the Smithsonian announced Tuesday.

Mr. Bunch, who began his career in 1978 at the Smithsonian’s Air and Space Museum, said in an interview that, as the Smithsonians’s 14th secretary, he hoped to figure out how to make the institution “more effective in the digital space” so that it could reach a broader audience than those who might have the time to visit Washington.

“I want to help it transform America,” he said.

As founding director of the African-American museum, Mr. Bunch led a decade-long effort to create a space that would recognize the achievements of black Americans, as well as the horrors of slavery and the struggle for civil rights. It fittingly opened on the National Mall in September 2016 at a ceremony at which President Barack Obama spoke.