In another seismic change for Washington theater, Howard Shalwitz, who in nearly 40 years at the helm has made Woolly Mammoth Theatre a national champion of the new — and frequently provocative — American play, will leave his post as artistic director in June 2018.

“It’s a pretty good run, 40 years,” Shalwitz said in a wide-ranging interview in his office above the playhouse on D Street NW. “Woolly is a theater that is always reinventing itself, that’s always taking leaps forward. But at a certain point, even that process is something you’ve done before.”

The 65-year-old Shalwitz, who has spent almost two-thirds of his life as Woolly’s artistic director, choked up several times during the interview, as he recalled the actors, directors, designers and playwrights who joined him on a career-long quest to expand the boundaries of what we think of as contemporary theater. That exploration gave Woolly license to go out on some wild limbs — leading to glorious triumphs as well as some jaw-dropping duds. But as in any dynamic art form, it is out there on the fragile, precarious leading edge that the most exciting new growth often occurs.

“Like the mascot that is its namesake, Woolly just insisted on being a very unique creature,” observed Mosaic Theater Artistic Director Ari Roth, who as head of Theater J staged four co-productions over the years with Shalwitz. “I admire Howard’s leadership in the most profound way. Because he stayed true to the mission, and he allowed the mission to change him.”

The mission took Woolly from ragtag roots — lacking its own space, it held its very first auditions outdoors, in Glover Park — to a $9 million, 250-seat theater in Penn Quarter that has won awards both for its design and the plays it has produced. Dramatists as varied as Nicky Silver, Danai Gurira, Sarah Ruhl and Branden Jacobs-Jenkins have been nurtured in Woolly’s rehearsal halls. The relationship Woolly forged with playwright Bruce Norris paid off in 2010, when his “Raisin in the Sun” spinoff “Clybourne Park,” got its start at Woolly and Playwrights Horizons in New York, and went on to win the Pulitzer Prize for drama.

Through its company-member model, the theater has been as responsible as any in the region for sustaining and fortifying a strong Washington acting community. And Shalwitz’s penchant for shattering expectations has guaranteed a Woolly show as a ticket to challenging the status quo.

“He looks long and hard at how can we not do what we’ve already done,” said John Vreeke, one of Shalwitz’s favorite directors. “That’s just part of his mental makeup. He refuses to repeat himself.”

A search for a new artistic director will begin shortly, organized by management arts consultant Greg Kandel and supervised by a committee that includes current and former trustees on the company’s 30-member board and other interested constituencies. Shalwitz will not participate directly in the process, he said, though it’s hard to imagine his voice not being heard, and loudly. He says he will meet with each candidate as the search narrows.

The announcement of his departure opens a second massive crack this year in the bedrock of Washington’s theater leadership. In February, another founding artistic director, Michael Kahn of Shakespeare Theatre Company, revealed the end date for his term of office, saying he would leave the classical organization at the conclusion of the 2018-19 season. With the retirement of Joy Zinoman at Studio Theatre several years ago, the stepping down of these other leaders will leave only Eric Schaeffer at Signature Theatre in place as a founding head of one of the region’s front-line theater companies.

As Shalwitz began in recent days to inform the actors, directors and board members who make up the Woolly family of his plans, those close to him tried to get their heads around the almost inconceivable notion of a Howard-less Woolly. “I don’t mean to get sappy or hyperbolic, but he is a father figure to me,” said Kimberly Gilbert, an in-demand actress whose career has been shaped by Woolly: since “Cooking With Elvis” in 2003, she has appeared in 17 company shows. “He is part of my art,” she added. “He is entrenched in it.”

“There’s a real loss at his leaving,” said Sarah Ruhl, a major dramatist embraced over the years by Shalwitz, who produced several of her plays, including the world premiere of “Dead Man’s Cell Phone.” “He has broad empathy, a very wide interest in human stories. And he has an aesthetic, a very particular one, but it’s also broad and inclusive.”

Shalwitz says that he’s been contemplating his exit for a few years: a committee was empaneled some time ago to deal with the possibility of his departure. It was the combination of the company’s sound fiscal health and round achievement numbers — the 2017-18 season will be his 40th — that persuaded him that it was a good time to move on. And he doesn’t think of himself as indispensable.

“Woolly’s much bigger than me,” he said. “It has been for a long time.”

If it truly is, Shalwitz is the main reason. With his good friend Roger Brady, a fellow actor, Shalwitz dreamed up the company in 1978. “We will resist the ossification which often accompanies institutionalization,” they wrote with youthful brio in their founding manifesto, “A Statement of Artistic Intent.” “When yesterday’s visions become today’s dogmas, art is dead.”

From a list of titles that ran several pages, they chose Woolly Mammoth as the company name during a long night of drinking in their apartment in Upper Manhattan.

“The only good answer was we were drunk,” Shalwitz said, about the name they settled on.

They’d soon move to Washington, where Brady only remained for a couple of years. But the name would stick memorably — as an indicator of something the opposite of extinct. It would connote a certain offbeat, renegade sensibility for a theater that didn’t intend to run with the pack. Woolly chose plays even if they’d been flops in other cities, and looked for playwrights with voices both fresh and outrageous: that’s what led Shalwitz to Silver, and his uproarious “Fat Men in Skirts” in 1991.

The company’s success with that play would underline its commitment to new work, and the kind of plays that sought to break the mold. Such was the case with the 2012 world premiere of Anne Washburn’s “Mr. Burns: A Post-Electric Play,” a stunning apocalyptic vaudeville inspired by “The Simpsons” that baffled as many theatergoers as it enchanted. He would also over the decade provide fairly steady employment to generations of fine actors who would be taken into the Woolly fold: actors such as Nancy Robinette, Michael Willis, Rob Roy, Grainne Cassidy and Grover Gardner in the early years. Later on, Sarah Marshall, Jennifer Mendenhall, Mitchell Hebert, Naomi Jacobson and Michael Russotto would come aboard, and on and on it went.

“Howard opened up not only the audience’s mind to what was available in the literary department. He also opened up the actor’s mind and what they were capable of doing,” said Rick Foucheux, who’s appeared in numerous Woolly shows, among them, the hit “Stupid F—ing Bird” that Shalwitz first directed in 2013.

Shalwitz still has a lot to say, and he hopes to get it all down in a book about the theater he’s planning to write. He also wants to direct some more and act a bit: he’ll appear, as a matter of fact, in the opening play of his final season, “The Arsonists.” In the meantime, he’s reflecting a lot on the blessings that have come his way. One of many that had him on the verge of tears was the recollection of a dinner not very long ago at the home of Arlene and Robert Kogod, who are major benefactors of many Washington arts institutions, Woolly among them.

“Arlene and Bob invited me to their home for dinner. I didn’t even know why!” Shalwitz recalled. “They said, ‘We want to give you a check for $2 million!’ ”

Just like that. It filled Shalwitz with wonderment, the notion that you could be a young buck, inventing a theater company over a bottle of wine and then over another bottle of wine decades later, be given a generous, tangible endorsement of what your labors have meant.

As he carried on a conversation with himself about that amazing gift, he choked up yet again.

“You mean, you said you were going to be with me, you said you believed in me, and now you’re going to back it up? With a check for $2 million?” Shalwitz’s voice rose as he reflected on his good fortune. “Who am I?” he asked.