Dunham talks to Emily Nussbaum at the New Yorker festival.

The hot ticket of this year’s New Yorker festival was a chat between Girls auteur Lena Dunham and New Yorker TV critic Emily Nussbaum. The 90-minute talk sold out long before events featuring lit stars Salman Rushdie, Zadie Smith and Martin Amis. When the conversation was opened up to the audience, fans stretched 20-deep up the two aisles.

One young woman complained that Girls didn’t completely capture her life. A self-described Shoshanna—the show’s insecure NYU student—excitedly wanted to tell Ms. Dunham about her new boyfriend. Another young woman, asking on behalf of her friends, wanted to know more about the generation that she insisted Ms. Dunham is a spokesperson for.

Nobody asked or especially seemed to care about Lena Dunham’s big news: that over the weekend, publishing houses were fighting over her new book, in a bidding war that wound up fetching $3.7 million.

Not That Kind of Girl is part memoir, part advice tome and the hottest literary property since Amanda Knox’s tell-all, which went to HarperCollins for $4 million last February. Ms. Dunham’s agent, Kim Witherspoon at Inkwell, invited incredulity when she opened bids last week at $1 million, but they shot up from there. Sarah Crichton, publisher of an eponymous imprint at Farrar, Straus and Giroux (and editor of We Killed by Yael Kohen and A Long Way Gone by Ishmael Beah) made it to $2 million before dropping out, leaving HarperCollins’s Ecco imprint and Random House to duke it out, according to sources.

On Monday morning, Random House Publishing Group announced that executive editor Andy Ward had won the prize.

“You don’t see proposals like hers very often,” Mr. Ward, a former GQ editor, said in a statement issued by the publisher. “Lena is so smart, so insightful, so funny, and so dedicated as a writer—dedicated in the best possible way. What more can you ask for as an editor?”

To spend that kind of fortune, Mr. Ward’s bosses at Random House must have a great deal of faith in their star wrangler, best known for the teary memo GQ editor in chief Jim Nelson sent out upon his departure from the magazine. That, and for editing The Secret Race, a recent timely title about the doping scandal in bike racing by Tyler Hamilton and Daniel Coyle.

BONUS:  The Lena Dunham Book Proposal—Reviewed!

To put Random House’s gamble in perspective, consider that an average first-time author is lucky to get $10,000, and $50,000 is considered a big deal. Her millions put Ms. Dunham firmly in the “can you believe that” clique, which includes Sarah Palin ($1.5 million author advance), Sarah Silverman ($2.5 million), Keith Richards ($7.7 million) and Hillary Clinton ($8 million).

“I’m obviously writing the wrong kind of books,” New Yorker editor in chief David Remnick joked when we asked him about Ms. Dunham’s windfall.

Lena Dunham was already having a big year, as the star, writer and showrunner of the HBO indie hit Girls. Hyped as “the voice of her generation” (or, as her character Hannah Horvath says, “a voice of a generation”), the 26-year-old Oberlin grad became a contributor to The New Yorker, bought an apartment in Brooklyn Heights, got five Emmy nominations and appeared on a billboard in Times Square. All this while being worshipped then lambasted then defended again in an endless back-and-forth in bars,  magazines and tweets. But is all that worth the price Little Random is paying?

According to publishing sources, the book would need to sell more than half a million copies between hardcover, paperback and ebook in order to be profitable for Random House, assuming an average cover price of $28. That would put it roughly in the same bracket as hits David Mitchell’s Cloud Atlas and Oprah’s revamped book club pick Wild by Cheryl Strayed.

In other words, expect to see more billboards. “With that kind of advance,” said Rob Spillman, the editor of Tin House magazine, “they are going to have to market the crap out of it.”

Little Random is positioning Not That Kind of Girl as Helen Gurley Brown meets David Sedaris and Nora Ephron, but it’s actually Tina Fey whom they should look to for sales comps.

The 30 Rock creator made headlines in 2008 when Little, Brown gave her a $5 million advance to write Bossypants. Although many at the time questioned that sum for a comic memoir, it was a book with a happy ending, selling 525,000 copies in hardcover and 265,000 in paperback, according to Bookscan (which only accounts for between 70 and 80 percent of sales), with ebook sales believed to be on par with the latter. The book topped the The New York Times’s bestseller list and stayed on for 23 weeks, a coup worthy of a Liz Lemon self high-five.

But Lena Dunham is no Tina Fey.

When Ms. Fey signed her deal, she had been the head writer for Saturday Night Live for almost 10 years, starred in the commercially released comedy Baby Mama and was Liz Lemon on NBC’s 30 Rock (which she also wrote and created). During its peak, 30 Rock averaged 7.7 million viewers.

“Tina Fey was a very known commodity,” Mr. Spillman said. “Lena is very culturally tapped in, but she has only done 12 episodes of a show that not that many people watched. I just don’t know where that extra audience is going to come from.”

The proposal for Not That Kind of Girl, mocked up to look like a charmingly vintage advice paperback book one might unearth in a thrift shop in an Ohio college town, includes sections on losing her virginity, diet, body image, crying at work, death and travel. The achingly self-conscious tone of the writing and many of the stories will be familiar to anyone who watches Girls, follows Ms. Dunham on Twitter or has read her in The New Yorker.

As demonstrated by the New Yorker Festival panel, Ms. Dunham does have fans who are willing to pay $30 to see her, and probably buy her book as well. Additionally, publishing insiders point out that the young audience she draws is influential, capable of fueling the type of online buzz that has helped propel Dunham’s rise, and thus highly desirable to advertisers.

“I hate to use the word ‘buzzy,’ but the show gets a lot of buzz,” said Casey Bloys, senior vice president of HBO Entertainment. “When a show starts conversations, that’s a good thing.”

But in the case of Girls, media chatter hasn’t translated into a monster hit.

The first season drew an average of 1.2 million viewers per episode, a modest success even by HBO’s standards, especially when compared with True Blood (5.8 million) and The Newsroom (2.8 million).

Its numbers are especially strong in East and West Coast urban enclaves: New York, Philadelphia, Boston, Portland and San Francisco. But the show hasn’t done well in the Midwest and the South.

“The goal of big media appearances is to start a national conversation, and she already has that going for her, so maybe there’s hope,” a publishing insider told us. “But she would have to expand interest in her brand beyond girls who graduated from liberal arts school, and I don’t really think that can be done.”

One book publicist likened Ms. Dunham’s appeal to that of twee writer and director Miranda July, in that “a select group of really talented, really interesting women will buy anything she does.” But, this publicist predicted: “That won’t be enough.”

At the New Yorker Festival talk, Ms. Dunham held court in a demure black dress, veering between talking about a recent appearance on a Fortune 500 panel and her feelings about her thighs. She talked about firing staffers and trusting her gut as a director rather than pesky actors “who haven’t eaten in four and a half weeks.”

Ms. Dunham came across as mature and confident, more bossypants than awkward Oberlin girl. She certainly looked nothing like her rumpled Girls alter ego Hannah Horvath, who also wanted to turn a collection of essays into a memoir, but couldn’t get even a modest book deal. In the first episode, her internship boss refused to even give her pages a look because she’d quit.

It is tempting to wonder what Hannah would think of her no-longer-scrappy creator, with her millions and her big-time book deal. Ms. Dunham and Random House can only hope that the Hannahs of the world buy a copy when it comes out.