The museum first opened its doors to the public in 1931, housed within a structure crafted by the architectural firm Sharp and Johnston.

Subsequently, in the late 2000s and 2010s, the museum initiated plans for a further relocation to a new facility situated in Larwill Park.

The Gallery's permanent collection serves as a repository of art for the Lower Mainland region, and has approximately 12,000 works by artists from Canada, and around the world.

[5] In 1938, the museum was one of the buildings occupied by unemployed protesters during a sitdown strike in the weeks leading up to Bloody Sunday.

[8] Renovations were also conducted to accommodate the 157 works bequeathed to the museum by Emily Carr, with the building reopened to the public in 1951.

[10] Before the re-purposed building was opened to the public, it was renovated by architect Arthur Erickson at a cost of CA$20 million, as a part of his larger three city-block Robson Square redevelopment.

Planning to relocate the museum began as early as 2004, a result from the gallery's need for more exhibition and storage space for its collections.

[11] However, Vancouver City Council later reversed its decision in April 2013, opting to approve the original proposed site in Larwill Park.

[15] The building was originally planned to be completed in 2020, and was named the Chan Centre for the Visual Arts after a major donor.

The design of the building includes ionic columns, a central dome, formal porticos, and ornate stonework.

A notable feature of the building is a pair of granite lions, placed on either side of the old entrance to the courthouse.

The building serves as the monthly meeting spot for Vancouver's Critical Mass, as well as flash mobs, the Zombie Walk, pro-marijuana rallies, and numerous environmental demonstrations.

In June 2021, Cheryle Gunargie created a vigil in honour of the unmarked remains of children discovered at the Kamloops Indian Residential School.

[30] As of December 2018, the Vancouver Art Gallery's permanent collection had approximately 12,000 works by Canadian, and international artists.

[31] The museum's collection of contemporary Asian art includes works by Eikoh Hosoe, Mariko Mori, Fiona Tan, Jin-me Yoon, Reena Saini Kallat, Song Dong, Wang Du, Wang Jianwei, Yang Fudong, and O Zhang.

[34] The painting Totem Poles, Kitseukla, by Carr, was among the original set of works acquired for the museum's collection prior to opening in 1931.

[27] The museum's also features a collection of indigenous Canadian art from the region, including works from Haida, Heiltsuk, Inuit, Kwakwakaʼwakw, Nuu-chah-nulth, Nuxalk, and Tlingit artists.

[41] Other works in the museum's indigenous Canadian collection includes works by Sonny Assu, Rebecca Belmore, Dempsey Bob, Dana Claxton, Joe David, Reg Davidson, Beau Dick, Brian Jungen, Marianne Nicolson, and Lawrence Paul Yuxweluptun.

[43] Its holdings include more than 50,000 books and exhibition catalogues, 30 journal subscriptions, 5,000 files that document various artists, art forms, and works.

In its most recent year, the gallery has featured over 60 presenters, including historian Timothy Brook, writer Sarah Milroy, and Emily Carr scholar, Gerta Moray.