Writers and photographers, like a young art student named Anne Leibovitz, would spend weeks on the road with their subjects, convincing bands like Fleetwood Mac to lay themselves bare.
"They were all sleeping with each other, and exchanging partners," recalled Wenner, "and there were fifteen different love affairs within the group and a lot of switching of beds. And that kind of so represented what was going on, and also was a brilliant solution, you know, to how to do a group cover, one of my favorites."
And the covers are what the magazine is most known for, those moments of vulnerability when artists open themselves up, either deliberately or not. But in the era of micro-managed, PR-savvy artists, these moments are becoming harder to capture.
"It's harder and harder," said Wenner. "I mean, unless the artist really wants to work with you ... we just want something that's sort of honest and real and interesting and provocative."
Despite this, the magazine still managed to collect a robust arrangement of covers in their catalogue, including the famous portrait of John Lennon, captured by Annie Leibovitz hours before his assasination.
"The picture was so powerful we didn't even put a headline on it on that magazine cover," Wenner explained. "I mean, it's the only time I've seen any magazine without a headline. You didn't need to say anything. It said it all. And out of respect to that, you didn't want to do anything to interfere with that image."
That precious distinction lasted until 1995, when Demi Moore appeared without a headline, simply for being famous.
Some saw this as a sign Wenner and the magazine had sold out. Wenner's used to the criticism and has heard it since he moved the magazine to New York in the mid-1970s and became as famous as his subjects.
Kurt Cobain summed it up when he wrote, "Corporate magazines still suck" on a T-shirt worn to Nirvana's first cover shoot for the magazine. He assumed Wenner would airbrush it out. He didn't.
"The fact of the matter is that he was on the cover, so no matter what his protest was, he was going along with it. [Why] would you bother to take out that statement, you know? And it made us, frankly, look bigger," said Wenner.
Wenner defends his mainstream migration as a reflection of America itself. Baby boomers grew up and values changed. Back then, John and Yoko's rear ends caused a stir. Today, rapper Kanye West photographed in a crown of thorns barely registers.
"These days, the most controversial is, why did you put Britney on the cover? She sucks," said Wenner. "But, you know, you can criticize Britney covers, but that is what teenage America looks at and goes 'We want to be like that.' You know, have her morals, her value."
And the opinion of a 61-year-old Wenner is still of utmost importance to kids with guitars and attitudes. The man who has documented the transformation of rock and roll remains remarkably nostalgia-free.
"If I sat here, I could tell you lots of stories but I don't dwell on the past that much," said Wenner. "I'm not sittin' around thinking, 'Oh, wasn't it great back in the day?' My kids always say back in the day to me. 'Dad! back in the day ...' Then I want to hit em!"