When Cameron Esposito takes the stage at her weekly Los Angeles standup showcase, Put Your Hands Together, she fuses the plucky charm of Amy Poehler, the assured storytelling of Louis C.K., and the self-deprecating shtick of Woody Allen. “How many days a week do you think a suburban girl should wear a coonskin cap?” she asks the crowd. “Because if you said zero, I went with seven. Still sort of wearing one, technically.”

She’s referring to her haircut, which she calls a side mullet. It’s far from the only thing to set this 32-year-old Chicago native apart. In a field dominated by men and fast-paced punch lines, Esposito narrates slow-building stories of suburban misadventures and gay weddings, all with wide-eyed charm and taut, edgy delivery.

Her comedy has won respect from her male peers and loyalty from her fans, who range from noisy beer swillers to indie comedy nerds. “Cameron exudes inclusiveness through her material and delivery,” says Mark Geary, founder of the Lincoln Lodge, the North Side comedy venue where Esposito once had a regular gig. “It’s that inclusiveness that people respond to so well.”

Much of her material stems from growing up a tomboy in suburban Western Springs and attending Catholic school in nearby Lisle. “We knew our neighbors, our neighbors’ neighbors, and our neighbors’ neighbors’ dogs,” says Esposito. “In the midst of this idyllic setting, I was a little gay kid with crossed eyes. You have to develop a great sense of humor in that situation.”

Eager to entertain, she signed up to be her high school’s football mascot (which involved wearing a giant red bird suit) and ran for student council. Esposito didn’t discover comedy until she started at Boston College, where she worked with an improv group even as she studied English and theology.

Two years after her 2004 graduation, the burgeoning comedian moved back to Chicago, where she started the Bucktown standup series The Spectacular Show. It was a bit of a stretch. “I’d never even done standup before,” she admits. “Like, I didn’t realize you had to have a mike. But I researched the best comics in the city and started booking them via MySpace from my parents’ den.”

Meanwhile, Esposito set about refining her writing and her routines, culling material from her religious upbringing (“I wanted to be a priest even though I was Catholic and that’s impossible”). Though she now considers herself an atheist, in standup she sees a clear connection to her religious roots. “[It’s] the power of getting together and delivering a sermon,” she says, “but without anybody going to hell.”

While Esposito was hosting Cole’s Open Mic in Logan Square and starring in a solo show, Side Mullet Nation, she watched a coterie of former Chicago comics, including Matt Braunger and Kyle Kinane, make their names in Hollywood. Last fall, she followed. “Chicago gave me the business savvy that I need to do my job in L.A.,” she says. “I’m proud to have come up there.”

After a year testing out her material in Los Angeles, which she has described as full of thin people “living off a diet of cigarettes and sad dreams,” she landed her big break: a September appearance on CBS’s The Late Late Show with Craig Ferguson. Another guest that night happened to be Jay Leno, the host of NBC’s The Tonight Show. Though she was nervous before her set, Esposito says, “I spoke with Jay before I went out onstage, and he was very kind to me.”

On the strength of such lines as “I thought all women wanted their boyfriends to come over and watch Buffy the Vampire Slayer then go right home,” she scored a regular gig on E! network’s Chelsea Lately. She’s also touring with Comedy Central star Anthony Jeselnik.

But despite her meteoric rise, Esposito still feels she’s got something to prove. “Most of the time when I walk out onstage, people don’t expect to see a tiny, side-mulleted lesbian,” she says. “They expect a comedian to look like Jerry Seinfeld; they expect a man. There’s an extra gulf that I have to close. But once I [do], they remember me.”

From the Mike

“I got engaged a few months ago, and as you can tell by my haircut, I will be marrying a woman. I didn’t always know I was a lesbian. I grew up in the suburbs of Chicago, and I didn’t know gay was a thing you could be. I thought gays were like leprechauns: mythical creatures for parades with special hats and buckles. I’m so happy to finally have a haircut and overall look that reflects my gender—my gender being fighter pilot—and to be marrying the gal of my dreams. What will we wear to the wedding? Two denim dresses. Obviously.”

On her haircut: “David Bowie needed someone to carry on his legacy.”

On being a lesbian: “I just thought all women had feelings for other women. Deep, deep feelings.”

Her denim collection: Includes 7 jackets, 2 vests, and 3 shirts.

Esposito performs November 26 through December 1 at Zanies; she is the featured performer 11/26 and 12/1, and she's a guest the nights of 11/27, 11/29, and 11/30. Tickets start at $15. For info, chicago.zanies.com