As a head-mounted display (HMD) designer at the University of Southern California Institute for Creative Technologies, Palmer Luckey earned a reputation for having the largest personal collection of HMDs in the world and was a longtime moderator in Meant to be Seen (MTBS)'s discussion forums.

The Oculus Rift prototype was demonstrated at E3 in June 2012. On August 1, 2012, the company announced a Kickstarter campaign to further develop the product.

Through MTBS's forums, Palmer developed the idea of creating a new head-mounted display that was more effective than what was currently on the market and was also inexpensive for gamers. To develop the new product. Luckey founded Oculus VR with Scaleform co-founders Brendan Iribe and Michael Antonov, Nate Mitchell, and Andrew Scott Reisse.

Oculus announced that the "dev kit" version of the Oculus Rift would be given as a reward to backers who pledged $300 or more on Kickstarter, with an expected shipping date set of December 2012 (though they did not actually ship until March 2013).

On December 12, 2013, Marc Andreessen joined the company's board when his firm, Andreessen Horowitz, led the $75 million Series B venture funding. In total, Oculus VR has raised $91 million with $2.4 million raised via crowdfunding.

In 2014, Samsung partnered with Oculus to develop the Gear VR, after the success of the then-in-development Rift.

Although Oculus only released a development prototype of its headset, on March 25, 2014, Mark Zuckerberg announced that Facebook, Inc. would be acquiring Oculus for US$2 billion, pending regulatory approval. The deal included $400 million in cash and 23.1 million common shares of Facebook, valued at $1.6 billion, as well as an additional $300 million assuming Facebook reaches certain milestones. This move was ridiculed by some backers who felt the acquisition was counter to the independent ideology of crowdfunding.

On March 28, 2014, Michael Abrash joined the company as Chief Scientist.

From 2014 through 15, two Innovator Editions (in-development versions of the Gear VR mainly sold to developers for sole research and understanding) were developed, manufactured, and sold. The device that the Innovator Editions used was the Note 4.

As of January 2015, the Oculus headquarters has been moved from Irvine, California to Menlo Park, where Facebook's Headquarters is also located. Oculus has stated that this move is for their employees to be closer to Silicon Valley.

In May 2015, Oculus acquired the British company Surreal Vision, a company based on 3D scene-mapping reconstruction and augmented reality. News reported that Oculus and Surreal Vision could create "mixed reality" technology in Oculus' products, similar to the upcoming HMD, Microsoft HoloLens. They reported that Oculus, with Surreal's help, will make telepresence possible.

On November 20, 2015, the consumer edition of the Gear VR was released to the public and sold out during the first shipments. The device supported the Samsung Galaxy Note 5, Samsung Galaxy S6, Samsung Galaxy S6 Edge, Samsung Galaxy S6 Edge+, and later, the Samsung Galaxy S7, and Samsung Galaxy S7 Edge.

Upon the acquisition of Oculus by Facebook Inc., Luckey "guaranteed" that "you won't need to log into your Facebook account every time you wanna use the Oculus Rift." Under its ownership, Oculus has been promoted as a brand of Facebook rather than an independent entity and has increasingly integrated Facebook platforms into Oculus products. Support for optional Facebook integration was added to Gear VR in March 2016, with a focus on integration with the social network, and integrations with features such as Facebook Video and social games.

The Oculus Rift CV1, also known as simply the Oculus Rift, was the first consumer model of the Oculus Rift headset. It was released on March 28, 2016, in 20 countries, at a starting price of US$599. The 6,955 backers who received the Development Kit 1 prototype via the original Oculus Rift Kickstarter campaign were eligible to receive the CV1 model for free.

In September 2016, support for optional Facebook integration was added to the Oculus Rift software, automatically populating the friends' list with Facebook friends who have also linked their accounts (displaying them to each other under their real names, but still displaying screen names to anyone else).

By 2016, the division began to be largely marketed as Oculus from Facebook.

On December 6, 2016, Oculus released motion controller accessories for the headset known as Oculus Touch.

On December 28, 2016, Facebook acquired Danish eye-tracking startup The Eye Tribe.

Following Facebook's acquisition of Oculus VR, ZeniMax Media, the parent company of id Software, and John Carmack's previous employer sought legal action against Oculus, accusing the company of theft of intellectual property relating to the Oculus Rift due to Carmack's transition from id Software to Oculus. The case, ZeniMax v. Oculus, was heard in a jury trial in the United States District Court for the Northern District of Texas, and their verdict was reached in February 2017, finding that Carmack had taken code from ZeniMax and used it in developing the Oculus Rift's software, violating his non-disclosure agreement with ZeniMax, and Oculus' use of the code was considered copyright infringement. ZeniMax was awarded $500 million in the verdict, and both ZeniMax and Oculus are seeking further court actions.

On October 11, 2017, Oculus unveiled the Oculus Go, a mobile VR headset manufactured by Xiaomi (the device was released in the Chinese market as the Xiaomi Mi VR). Unlike the Oculus Rift, the Go is a standalone headset that is not dependent on a PC for operation. Unlike VR systems such as Cardboard, Daydream, and the Oculus co-developed Samsung Gear VR (where VR software is run on a smartphone inserted into a physical enclosure, and its screen is viewed through lenses), it contains its own dedicated display and mobile computing hardware. The headset includes a 5.5-inch 1440p fast-switching LCD display, integrated speakers with spatial audio and a headphone jack for external audio, a Qualcomm Snapdragon 821 system-on-chip, and 32 or 64 GB of internal storage. It runs an Android-based operating system with access to VR software via the Oculus Home user experience and app store, including games and multimedia apps. The Go includes a handheld controller reminiscent of one designed for the Gear VR, which uses relative motion tracking. The Oculus Go does not use positional tracking.

The initial Oculus headsets, produced under the "Oculus Rift" brand, are traditional VR headsets that require a PC to operate. In 2018, Facebook CEO Mark Zuckerberg stated that the original Oculus Rift "CV1", Oculus Go (a lower-end standalone headset released in 2017), and first-generation Quest were the company's first generation of products, and expected new iterations of the three to be developed for a second generation of the company's technology.

Facebook announced in August 2018 they had entered negotiations to lease the entire Burlingame Point campus in Burlingame, California, then under construction. The lease was executed in late 2018, and the site, owned by Kylli, a subsidiary of Genzon Investment Group, was expected to be complete by 2020. Oculus was expected to move to Burlingame Point when development is complete.

In September 2018, Oculus became a division of a new structural entity within Facebook known as Facebook Technologies, LLC.

On September 26, 2018, Facebook unveiled Oculus Quest. It was originally unveiled as a higher-end counterpart to the Oculus Go, and part of a goal to reach one billion VR users. Similar to Oculus Go, it uses embedded mobile hardware running an Android-based operating system, including a Snapdragon 835 system-on-chip, and 64 or 128 GB of internal storage. The Quest uses OLED displays with a resolution of 1600x1440 per eye and running at 72 Hz. It supports Oculus Touch controllers via an "inside-out" motion tracking system known as "Oculus insight", which consists of a series of cameras embedded in the headset. The controllers were redesigned to properly function with Insight. It supports games and applications downloaded via Oculus Store, with ported launch titles such as Beat Saber and Robo Recall. It also supports cross-platform multiplayer and cross-buys between PC and Quest. Facebook stated that they would impose stricter content and quality standards for software distributed for Quest than its other platforms, including requiring developers to undergo a pre-screening of their concepts to demonstrate "quality and probable market success".

On March 20, 2019, at the Game Developers Conference, Facebook announced the Oculus Rift S, a successor to the original Oculus Rift headset. It was co-developed with and manufactured by Lenovo and launched at a price of US$399. The Rift S contains hardware features from the Oculus Go and Oculus Quest, including Oculus Insight, integrated speakers, and a new "halo" strap. The Rift S uses the same 1440p fast-switching LCD display and lenses as the Oculus Go (a higher resolution in comparison to the original model, but lower in comparison to Oculus Quest), running at 80 Hz, and is backward compatible with all existing Oculus Rift games and software. Unlike the original Oculus Rift, it does not have hardware control for inter-pupillary distance.

Oculus began to phase out the original Oculus Rift "CV1" in 2019, in favor of Oculus Rift S — a follow-up to the original model manufactured by Lenovo that incorporates elements of the Go and Quest.

On August 13, 2019, Nate Mitchell, Oculus co-founder and VP of product announced his departure from the company.

In November 2019, Facebook released a beta for a new feature known as Oculus Link, which allows the Quest to be attached to a PC over USB 3.0 for use with Oculus Rift-compatible software.

On November 13, 2019, John Carmack wrote in a Facebook post that he would step down as CTO of Oculus to focus on developing artificial general intelligence. He stated he would remain involved with the company as a "Consulting CTO".

Oculus Go was declared end-of-life in June 2020, with software submissions to end in December 2020, and firmware support ending in 2022.

On August 18, 2020, Facebook announced that all "decisions around use, processing, retention, and sharing of [user] data" on its platforms will be delegated to the Facebook social network moving forward. Users will soon become subject to the unified Facebook privacy policy, code of conduct, and community guidelines, and all users will be required to have a Facebook account to access Oculus products and services.

Standalone account registration became unavailable in October 2020, all future Oculus hardware (beginning with Oculus Quest 2) only supported Facebook accounts, and support for existing standalone Oculus accounts on already-released products will end on January 1, 2023. Facebook stated that this was needed to facilitate "more Facebook powered multiplayer and social experiences" and make it "easier to share across our platforms". Facebook stated that users would still be able to control sharing from Oculus, maintain a separate friends list within the Oculus platform, and hide their real names from others.

Users and media criticized Facebook for the move. Ars Technica noted that there is no clear way to opt-out of information tracking and that the collected data will likely be used for targeted advertising. Furthermore, Facebook requires the use of a person's real name. In September 2020, Facebook temporarily suspended sales of the Oculus Quest in Germany; a German watchdog had presented concerns that this integration requirement violates the General Data Protection Regulation (GDPR), which prohibits making use of a service contingent on consenting to the collection of personally identifiable information, and the requirement that existing users also link to a Facebook account to use Oculus hardware and services.

In September 2020, Facebook unveiled an updated version of the Quest, Oculus Quest 2. It is similar to the original Quest, but with the Snapdragon XR2 system-on-chip and additional RAM, an all-plastic exterior, new cloth head straps, improved Oculus Touch controllers with improved ergonomics and battery life, and an 1832x1920 per-eye display that is currently supporting running at 120 Hz. Similar to the Rift S, it uses a single display panel rather than individual panels for each eye. Due to this design, it has more limited inter-pupillary distance options than the original Quest, with the ability to physically move the lenses to adjust for 3 common IPD measurements. The Quest 2's models are both priced US$100 cheaper than their first-generation equivalents.

On September 16, 2020, the Rift S was discontinued in favor of the Oculus Quest 2.

In June 2021, Facebook announced it would do a test launch of targeted advertisements in applications for Oculus Quest. The company claims that movement data, voice recordings, and raw images from the headset will not be used in targeting. Instead, the ads will rely on information from the user's Facebook profile and all user activity related to Oculus - installing apps, viewing content, subscription to apps, adding an app to the checkout cart or wishlist. The company has not stated whether ads will appear only in applications or in the Oculus Home experience as well.