Eric Avery was born in Los Angeles, California. His father is the actor Brian Avery, perhaps best known for playing Carl Smith (who Dustin Hoffman famously keeps from marrying Katharine Ross) in The Graduate.
Avery and Dave Navarro met as classmates at St. Paul the Apostle Grammar School in West Los Angeles, a Catholic parochial school founded by the Paulist Father. Eric went on to St. Monica High School of Santa Monica, California, and Dave Notre Dame High School in Sherman Oaks, California. Dave was classmates at Notre Dame with Stephen Perkins. Stephen met Eric's sister, Rebecca Avery, and they dated. Rebecca suggested that Eric and Perry Farrell audition Stephen as the drummer for Jane's Addiction after Perry and Eric cofounded the band.
Avery kept a fairly low profile after the first demise of Jane's Addiction, participating in the Deconstruction project with Navarro immediately after Jane's Addiction's breakup, but initially declining invitations for Jane's reunions. "I've asked him," said Farrell before 2001's Jubilee Tour, "but he says he wants no part of it. What else can you say but, Good luck to ya?"
Avery has recorded tracks for, toured with and briefly dated Alanis Morissette, as well as creating another side project, Polar Bear, in 1994. He was once suggested as the replacement bassist for Tool by former Jane's Addiction and then-current Tool manager Ted Gardner. Eric declined the invitation, saying he wanted to concentrate on Polar Bear.
As seen in the film Metallica: Some Kind of Monster, Avery auditioned for Metallica, after the departure of bassist Jason Newsted. The role didn't quite fit Avery and the band went with Ozzy Osbourne and Suicidal Tendencies bassist Robert Trujillo. Avery toured with the band Garbage to promote 2005's Bleed Like Me. Avery has also performed with Peter Murphy, on tour and on 2004's Unshattered.
Avery worked briefly with the revived Smashing Pumpkins, but ultimately did not join the band. He was not paid for his work, but said the sessions were a lot of fun: "I went into [the Pumpkins] with the same mentality I took with me when I auditioned for Metallica – I expected to have a good story to tell my wife. I had no expectations. I had heard nothing but bad things about working with Billy, but I went, and I found it to be a really inspiring time." Billy Corgan ended up playing bass on what would become 2007's Zeitgeist and hired Ginger Reyes for live performances.
In 2007, he contributed original music to the feature film documentary The 11th Hour. He also released his debut solo album Help Wanted in April 2008 through Dangerbird Records.
He finally performed with Jane's Addiction – for the first time since 1991 – at the NME Awards in 2008. Jane's played secret club shows in October and November 2008. On March 19, 2009, at South by Southwest Music festival in Austin, the quartet performed a 45-minute set at an abandoned Safeway grocery store.
Jane's Addiction's official website was updated in February 2009 stating that there was to be another club show soon. Photos of Avery, Perkins and Navarro, taken by Trent Reznor, appeared on Nine Inch Nails' official site, which led to speculation that Reznor was helping Jane's record new material. The relationship led to the booking of the "NIN/JA" (Nine Inch Nails/Jane's Addiction) tour, on which Avery played, and which evoked the first Lollapalooza tour of 1991, starring Jane's and Nine Inch Nails.
On March 1, 2010, after a 10-date rescheduled tour in Australia, Avery stated on his Twitter page: "the janes addiction experiment is at an end." Rumors were already spreading around a few weeks before, as Duff McKagan was said to be the new bassist for Jane's, but Avery had kept his position for the remaining few dates of the 2009/2010 tour.
In February 2012, Justin Meldal-Johnsen commented on the talkbass.com forum that Avery would be joining Garbage on their upcoming tour. In early May 2012 Garbage uploaded a video from their rehearsal, performing the song "Battle in Me", with Avery playing bass. Avery has since performed in the two Garbage tours that followed, the band's 20th anniversary tour and the one for the album Strange Little Birds, in which Avery plays bass in six tracks.
Avery released his second solo album, entitled LIFE.TIME., on February 15, 2013.
On February 25, 2013, Trent Reznor named Avery as the new touring bassist of Nine Inch Nails. Avery was slated to perform in the Twenty Thirteen Tour from Summer 2013 into 2014, but announced his withdrawal on May 15, 2013, stating that after a year travelling with Garbage he did not feel like going on another extended tour.