The Bronx native joined the Santa Monica-based public radio station in 1977 when it had five employees and the oldest transmitter west of the Mississippi.
The departure of Boilen, who also created and hosts All Songs Considered, follows news that two other high-level executives will soon exit the broadcaster.
The programming head, who helped make the Tiny Desk concert series a phenomenon, will exit her role at the end of the year.
"We are not putting our journalism on platforms that have demonstrated an interest in undermining our credibility."
The popular podcast crafted a lopsided contract and released an obscure track in an attempt to "explain the music industry."