Jon Bakhshi began his career as a club promoter. In July 2005, he entered the entrepreneurial field when he opened Home, a nightclub on West 27th Street in Chelsea, Manhattan. He opened a nearby companion club called Guest House in August 2005. Both clubs were housed on the second floor of the Twilo Building. Bakhshi's clubs distinguished themselves from other clubs in the area by maintaining less strict entry requirements. Guest House was open 5 days each week while Home stayed open for 6 days a week. In July 2009, Bakhshi closed both Home and Guest House.

In 2008, Jon Bakhshi began setting into motion construction on an "eco-friendly" SoHo nightclub. Prior to opening, Jon Bakshi held publicity parties at the Cannes Film Festival, Sundance Film Festival, and Paris Fashion Week. The latter party was hosted by models Jessica Stam and Carmen Kass at Le Baron, a club in Paris. Bakhshi worked with architect, Antonio Di Oronzo, on the design of the Varick Street club. It featured hick bamboo walls, LED lighting, sustainable uniforms for employees, wind-generated electricity, waterless urinals, and vodka served in recycled bottles. It featured two levels on which differing styles of music could be played simultaneously. The club was also the first LEED-certified nightclub in the United States. The club officially opened in October 2008. Greenhouse would eventually close in April 2014.

In October 2009, Jon Bakhshi opened a restaurant/nightclub called Juliet Supperclub in Chelsea. The location featured a Mediterranean theme and menu. It was closed in 2012. Famous  Chef and restaurateur Todd English created the menu for Juliet in 2009.

In April 2014, Bakhshi opened a combination bar, restaurant, and secret nightclub called Beautique on Manhattan's 58th Street. The establishment has made headlines for the notability of some of its guests. Celebrities like Leonardo DiCaprio, Kate Bosworth, Dylan McDermott, and many others have gone to Beautique. It won the Concierge Choice Award for Best New Restaurant in New York City in 2014. In May 2015, Bakhshi opened a second Beautique location in The Hamptons at the Capri Hotel. Known as a celebrity hot spot, a-listers such as Jennifer Lopez, Kevin Spacy, Martha Stewart, Joaquin Phoenix and Howard Stern frequently dine there.