Breaks like this are usually one-shot deals, but the BSO kept calling back. Another boy choir, for performances of Mahler's Third Symphony, in 1966. Then an offer to be Leinsdorf's assistant conductor for vocal and choral activities during the 1968 and '69 Tanglewood seasons.

Finally, Oliver put it straight to the orchestra's administration: "The Boston Symphony doesn't have a chorus, and they need a chorus," he told them. "It should be called the Tanglewood Festival Chorus. And I'm the guy."

(If that sounds a bit presumptuous for a guy under 30, consider that Oliver had been earning a paycheck as an organist or choral conductor since he was 11, and says now that he has never been unemployed as one or the other.)

"And to my great astonishment then, and even greater now," he continued, "they took me up on it and said, sure, give it a try."

The rest, as they say, is history. The Tanglewood Festival Chorus made its debut on April 11, 1970, in a Symphony Hall performance of Beethoven's Ninth Symphony under Leonard Bernstein. Over the years it has gone from a pickup group of 60 to an ensemble with a roster of 320, serving not only the BSO but the Boston Pops, as well as giving its own concerts. Its ranks include some of Boston's best singers, and though it rivals similar professional — that is, paid — groups for polish and lucid diction, it has proudly remained a volunteer group whose members sing because they want to, a key facet of Oliver's vision.

The numbers are staggering: Some 2,200 choristers have sung in the TFC in more than 2,000 performances at home and on tour, all prepared by Oliver over the course of 46 seasons.

And now, he's done.

Oliver will step down from the TFC on Sunday, when it gives its final performance under his guidance. In a neat bit of symmetry, his BSO career will end as it began: with Beethoven's Ninth Symphony, under the baton of guest conductor Asher Fisch. Before the performance, Oliver will be presented with the second Tanglewood Medal in recognition of service and achievement. (The first was awarded to Seiji Ozawa in 2012.)

"John's always delivered, even under the toughest circumstances," said Tony Fogg, the BSO's artistic administrator. "And I think that's been a very important quality to his work and his profession. John has kept a level of musical and artistic draw that has maintained that big corpus of singers for many, many years now."

He still has a lot of energy, too — you sense it even over the phone. So why leave now?

"My standard answer to that is: ticktock," says Oliver with a laugh. "I'll be 80 in four years." He's grown exhausted of commuting between homes in Western Massachusetts and Boston. "I'd love to be my own gardener again, instead of just pointing for other people," he said. He plans to write books, among them a memoir and a Southern Gothic comedy novel. And even for someone with his commitment to music, there's now a certain been-there, done-that quality to his career.

Most important, the working out of the relationship between a choral conductor and music director takes years — a whole decade in the case of Ozawa, he said — and at his age, he doesn't feel he has those years to devote to the process anew.

"I like him very much and he's extremely able," Oliver said of Andris Nelsons. "But it would take a long time for us to read each other's mind the way Seiji and I did."

"I truly admire John Oliver's tremendous achievements as conductor of the Tanglewood Festival Chorus since 1970," said Nelsons in a statement from the BSO. "The TFC is very much regarded for its dedication to excellence in performance, impressive commitment to a rigorous work schedule, and generosity in giving their time and skill to the BSO, and I know John Oliver has been such an essential source of inspiration for them. I sincerely thank John for his years of service, and I wish him the very best following his remarkable career with the TFC and BSO."

Serving as an orchestra's choral conductor is a funny thing. You don't ordinarily control the repertoire, and despite the fact that you've prepared a major aspect of a piece, someone else usually gets up on the podium and grabs the attention and most of the credit. It rankles some very talented conductors.

Oliver, though, had his own ensemble and various groups around Boston, where he could tackle whatever he pleased. That meant that "he could always eat his ego and prepare the chorus in a way that Colin Davis, say, could come in and put his stamp on it," said tenor Henry Lussier, who met Oliver in 1971 at MIT, joined the TFC the year after, and has been there ever since. "That didn't hurt his feelings, because he had many outlets beyond that."

It freed him up to enjoy collaborating with a long line of BSO music directors and guest conductors. Rafael Frühbeck de Burgos was a treasured friend and frequent dinner guest. So was Davis — he and Oliver were both young men at the beginning of their BSO associations.

"We fought like cats and dogs," said Oliver, who remembers sitting in the Amalfi restaurant with Davis at 2:30 in the morning during a blizzard. "He was drinking his favorite, hot tea with rum. I don't remember what I was drinking — probably scotch by that hour. And we were sitting there arguing about what this or that dynamic meant to Berlioz. And we had such fun."

And then there are the stories that open a window onto a different era in the BSO's history. Oliver was in Ames, Iowa, with William Steinberg for a 1972 performance of Brahms's "German Requiem." Over burgers at a local diner, Steinberg pointed to one side of his nose and told Oliver, "This side is the Jewish side." Then he turned and pointed to the other and said, "This side is the side I show to the trustees."

Some performances stand out too, like the time Gunther Schuller programmed Luigi Nono's insanely complex "Il canto sospeso" before the TFC was even a year old. "We weren't ready for that at all. But we were game. And that's what Gunther loved — he loved somebody that would take a challenge and go for it." And Schoenberg's opera "Moses und Aron" under James Levine, who never conducted the chorus when he came for piano rehearsals. "He always had me conduct, and he invariably said to me, 'You conduct that better than anyone in the world.' Didn't matter what the piece was."

It is not lost on Oliver that many of his closest BSO colleagues — Frühbeck, Davis, Schuller — are gone: an acute reminder of time's passage. Likewise a set of performances of Beethoven's "Missa Solemnis" in 2012, for which Oliver substituted at short notice for an ailing Kurt Masur. "What I found the most difficult thing was, I really had trouble walking from the podium into the wings at the end," he said. "I was physically exhausted. That's one of the things that told me, time has elapsed. You're getting older, you know?"

And so he will bow out, leaving to his successor an ensemble that performs largely from memory and needs virtually no drilling of notes, even for complex scores. It is, Lussier said, a group that shows up knowing the music, already eager to pass beyond it and go more deeply into its essence.

"John always made you feel like he was bringing the best out of you, and never in a dictatorial way," Lussier said. "He just brought you up to another level, and everyone was a colleague. So we all felt better after the process — about ourselves, about our singing. And some conductors aren't like that."

Whoever takes Oliver's place will undoubtedly do things differently. But if he or she preserves that spirit, his legacy will be secure for some time.

Boston Symphony Orchestra

Asher Fisch, conductor

Music of Copland and Beethoven

At: Tanglewood, Lenox, Sunday at 2:30 p.m.

Tickets: $20-$97.

617-266-1200, www.tanglewood.org

David Weininger can be reached at globeclassicalnotes@gmail.com. Follow him on Twitter @davidgweininger.