During the final show of Dead & Company’s so-called Final Tour on Sunday night, the crowd at Oracle Park in San Francisco swayed and bobbed like the current of a turning river.

People in flower crowns grooved through the shimmying mass on the stadium’s field. A man in cowboy regalia cupped his hands around his ears and two-stepped to the beat. A woman in face glitter who gave her name as Honey Bee regaled strangers with the tale of how she came with a man she had met two days before, who happened to have an extra ticket. Other fans, who were not as lucky, danced on the sidewalk outside of the park.

And onstage, the band’s lead guitarist, John Mayer, leaned back, sucked his lips inside his mouth and scrunched his eyes closed as he wailed on a guitar while playing the song “Althea.” Shortly after his impassioned solo, footage of it started spreading on Twitter.

Mr. Mayer has been a member of Dead & Company, an offshoot of the Grateful Dead, since it formed in 2015. Though he is not the band’s face, the faces he has made while performing — which can cover the full spectrum of human emotion, from despair to sweet relief to sublime pleasure — have for some been almost as unforgettable as the music itself.

Fans have made YouTube compilations, photo collages, a meme with a giant slug and niche Instagram accounts dedicated to Mr. Mayer’s expressive “guitar face,” which is not exactly an anomaly in the world of rock ’n’ roll. “I feel a little bit uncomfortable with people thinking that I made up the guitar face,” he told Rolling Stone in 2017. “God, wouldn’t it be great to go to the jungles of Borneo and give a tribe Fender Stratocasters and have them listen to Jimi Hendrix — but not show them Jimi Hendrix — and come back five years later and see if there’s any guitar face? I have a feeling there would be.”

Mr. Mayer, through a representative, declined to comment for this article. The faces he made during the last leg of the Final Tour appeared to reflect the mood of its tie-dye-wearing fans, which alternated between grief and ecstasy as the music that seemingly would never stop finally did. (Dead & Company members have said the tour would be its last, but have not ruled out the possibility of a future for the band.)

“The thing I love about him is he’s fully enjoying it — he’s in the music,” Tony Seigh, from Valparaiso, Ind., said of Mr. Mayer. “For those three, four hours, that guy is just in a different zone. And haters beware, he’s going to be making some very strange faces.”

Mr. Seigh, 33, runs Holy Moly Mischief, which sells Dead-themed T-shirts, fanny packs and a bumper sticker that reads: “KEEP HONKING! I’m on my way to see JOHN MAYER and what’s left of the GRATEFUL DEAD.” Mr. Seigh, who used to work for Tesla, said he had seen Dead & Company 86 times, and he described Mr. Mayer’s faces using a word many others did: orgasmic.

“It’s like a close-up of his face in an adult film,” he said. “There are moments where it’s like, Oh my gosh, something is happening to him. Like, is a ghost … massaging him?”

Mr. Seigh, who was wearing a yellow “Always Grateful” hat that matched his yellow-painted toenails, added that Mr. Mayer’s expressions were one of many visual elements of live performances by Dead & Company, whose members have included Bob Weir, Oteil Burbridge, Mickey Hart, Bill Kreutzmann, Jeff Chimenti and Jay Lane.

“Bob looks like a gray werewolf, and Oteil has, like, pro-wrestler face paint on, and Mickey looks like ET playing some drum thing,” he said. “And then you look at John, and he looks like pictures of old Catholic saints when they’re getting visited by an angel.”

Clif Edwards, 60, a graphic designer from Sacramento whose hair was styled into a long gray ponytail, said that as a guitarist himself, he knew how playing could be a full-body experience. Of Mr. Mayer’s facial expressions, he said, “I approve.”

“But it’s odd to watch,” added Mr. Edwards, who said he had seen the original Grateful Dead play some 340 times.

A man in a tie-dye bucket hat who was standing near Mr. Edwards chimed in: “You know you’re in the thick of the jam when he’s got the face going.”

Susan Marston, 58, a program manager from Boise, Idaho, said that unlike some longtime Dead fans who were skeptical when Mr. Mayer joined Dead & Company, she knew from the very beginning that he would bring something unique to the spinoff band.

“There’s a lot of crusty people who said, ‘Oh, I can’t see John Mayer,” Ms. Marston said. “But if you knew anything about John Mayer prior to joining Dead & Company, then you knew the guy could freaking rip the blues.”

“Sometimes his eyes are rolling back in his head,” added Ms. Marston, who was wearing a black top covered with photos of Mr. Mayer. “It elevates everybody because he’s so into what we’re into — it’s our synchronization with the band.” As she spoke, a man with a fake scarlet begonia tucked into his hat interrupted her to show off a sticker that featured Mr. Mayer’s face flashing a particularly euphoric expression and surrounded by a highly suggestive lyric from the song “The Weight.”

A few Dead & Company fans said they had never noticed Mr. Mayer’s expressions. Kim Holzem, 52, from Three Rivers, Calif., scoffed in disbelief when her husband, Tim, mentioned that he had never registered the guitarist’s faces before.

“Sometimes he looks like he’s in pain, other times he looks like he’s blissed out,” said Ms. Holzem, who saw Dead & Company three times last weekend in San Francisco with her husband and two teenage sons.

Mr. Mayer, she added, “makes some weird-ass faces, but he’s still adorable.”

Skyler McKinley, 31, a bar owner from Denver who was standing not far from the stage at the last show of the tour, said Mr. Mayer’s face was “inescapable” at live performances, in part because it is often “blown up, to skyscraper size” on massive screens. He added that Mr. Mayer had the “sex energy of a rock star” while performing, and compared his facial expressions to the dance moves of Mick Jagger.

“At first I thought it was absurd, these lewd faces,” Mr. McKinley said. “But this is his aspect of communing with Grateful Dead music, the same way we all do, in a religious sense.”

“I have no idea what my face looks like when I’m at one of these shows,” he added, “but I bet I look pretty ridiculous, too.”