The club opened in 2017 and is co-owned by actor Alan Cumming and promoter Daniel Nardicio, who founded it with the owners of the space's previous establishment.

The line-up is ... eclectic and edgy with weekly stand-up comedy (Wednesday’s Cabernet Cabaret), sexy 'boylesque,' drag revues, and plenty of surprise guests.

[4][5] One of the murals features Nashom Wooden, a longtime staple of the New York City queer nightlife scene, alongside Daniel Nardicio, a local promoter who is also co-owner of the bar.

[6] Of Club Cumming's clientele, The New York Times said, "On a recent Saturday night, the crowd was a tightly packed mix of neighborhood gay men in vintage T-shirts brushing up against Becky types in black and gender-non-conforming millennials wearing glittery tanks, colorful scarves and the occasional boa.

[7] Every night features at least one event,[8] among the most common of which are live music, DJ sets, lounge acts, drag shows, go-go dancing and "raunchy readings".

[7] Club Cumming is a popular stop for celebrities who visit New York City, and Broadway actors frequent the venue on Mondays, when their plays typically do not run.

[19][20][22] The week it opened in September 2017, Paul McCartney, Emma Stone and Cumming gave an impromptu performance of "Part of Your World" while spending an evening there.

[14][17][23] Since then, figures including Justin Vivian Bond, Billie Jean King, Adele, Jennifer Lawrence and Vanessa Williams have also made appearances.

[3][29] The first installment featured comedians Bowen Yang, Pat Regan, Mitra Jouhari, Sydnee Washington, Rachel Sennott and Joel Kim Booster.

[28][30] During the June 2020 George Floyd protests in New York City, the venue operated as a safe haven for Black Lives Matter protestors, providing shelter, first aid, and supplies like water and personal protective equipment.

[31][32] Cumming donated a portion of the Community Chest's funds to Black Lives Matter, and the club, which was not in the direct path of any protests, also stored supplies for demonstrators.

[33][34] The seminal event was a two-night variety show hosted by Cumming; it featured performances by Kim David Smith, Catherine Cohen, Michael Musto, Alexis Michelle, Detox and Jill Sobule.

In 2019, it won the title of Best Bar at the Glam Awards, an annual ceremony à la the Oscars for queer entertainers, promoters and venues in New York City.