In 1969, the centre assumed management of the newly constructed State Film Theatre, providing a facility for exhibiting material not screened in commercial cinemas.

The program provided screenings for Victorian Certificate of Education students, based on core texts, and in-service days for their teachers.

In July 1997, following an open, international and two-stage design competition, Lab Architecture Studio (based in London at the time), in association with their joint venture partners, Bates Smart architects, was announced as the winner.

The first stage was opened in October, with two exhibitions, Deep Space: Sensation & Immersion and Ngarinyin Pathways Dulwan, running in ACMI's Screen Gallery.

[6] The Screen Worlds exhibition was opened by Cate Blanchett, who loaned[7] her Oscar for best supporting actress for her part as Katharine Hepburn in The Aviator.

[9] ACMI partnered with Melbourne architectural firm BKK Architects, who redesigned the museum's functional layout and public spaces.

[12] ACMI partnered with Melbourne chef, restaurateur, writer and television presenter Karen Martini and Michael Gebran of HospitalityM to launch its restaurant, bar and café Hero.

[16] After a period of turmoil, with the organisation over budget,[17] Smithies left ACMI in 2004,[16][18][19] and later said the facility had been forced to open while "under-funded" by the Victorian Government.

He directed the museum's Imaging Frontiers masterplan re-development, which generated record visitor numbers and international critical acclaim.

ACMI's 1,600sqm centrepiece exhibition explores the past, present and future of film, television, videogames and art, and features over 900 objects from around Australia and the world.

[28] The Story of the Moving Image begins with objects and interactive experiences that showcase people, techniques and inventions that contributed to the development of motion pictures.

Costumes, characters, set and production design, storyboarding, visual effects and Foley are featured in the Moving Worlds section to illustrate the creative processes behind iconic films, TV shows and videogames.

[29] Moving Minds encompasses factual media and information that traverses the history of newsreels, broadcast TV, documentary, war reporting and propaganda, citizen journalism and video art.

The Lens[32] is a handheld, take-home device that lets visitors collect artworks and objects throughout The Story of the Moving Image and other select exhibitions hosted at ACMI.

[28][33] The Lens can be used at the Constellation, a room-scale experience located at the end of The Story of the Moving Image exhibition, consisting of six interactive touchscreen tables with an interface developed by Grumpy Sailor and a data visualisation designed by OOM Creative and More Studio.

The Constellation takes the items collected by visitors on their Lens devices throughout the exhibition and connects them up to hundreds of other films, TV series, artworks and videogames beyond the scope of the gallery.

[37] Referenced screen works include major films such as Titanic, Blade Runner, and Star Wars: The Empire Strikes Back, and television shows such as The Simpsons, The Wire, and The X-Files.

[38] Visitors can add sound effects to scenes from Round the Twist and Li'l Elvis and the Truckstoppers using unconventional objects typically used in the practice of Foley art.

Highlights have included seasons on Wong Kar-wai, Agnès Varda, Abbas Kiarostami, Dario Argento, William Klein, John Cassavetes, and Jim Henson.

Genres have included Ozploitation; Zombie Horror; East German Cinema; and Monsters, Ghouls and Melancholy Misfits in conjunction with the Tim Burton exhibition.

[123] Beginning with Mary and Max, which toured regional Victoria,[124] ACMI then followed by showing the 2011 Best of the Independent Games Festival [125] in Sydney and Brisbane; Shaun Tan's The Lost Thing: From Book To Film[126] and War Pictures: Australians at the Cinema 1914–1918;[127] and ACMI's first original exhibition in the Melbourne Winter Masterpieces series, Game Masters: The Exhibition.

[189] ACMI's main YouTube channel publishes recorded talks, interviews with artists, season trailers, screen culture essays and behind-the-scenes videos.

Commissioned artists include Lu Yang, Matthew Griffin, Ross Gibson, Jazz Money, Moorina Bonini, Kalanjay Dhir, Laura Duffy, Firepit Collective, Xanthe Dobbie, APHIDS, Daniel Jenatsch, Oliviah Koh and Emile Zile.

[194] ACMI publishes essays, interviews, recorded talks, behind-the-scenes videos, topical articles and recommendations related to film, television, videogames and digital art on its website.

[195] An abridged online version of ACMI's centrepiece exhibition, The Story of the Moving Image, was launched in October 2020.The Story of the Moving Image Online is presented in six parts: Australian Television, Australian Film, Videogames, Blak Women on Screen, Social Video and Digital Art.

[201] Located in Fed Square, ACMI's restaurant, bar and café Hero featured a menu developed by Melbourne chef, restaurateur, writer and television presenter Karen Martini.

[203] The ACMI X Industry Residency program provides an office space, resources and networking opportunities for Melbourne-based creative practitioners, startups and businesses working across film, TV, videogames and art.

Screen Worlds explored the story of the moving image through a number of different sections – Emergence, Voices, Sensation, Games Lab and Kids Space.

The Memory Grid was a display allowing access to over 100 hours of film that were recorded by ordinary Australians, independent filmmakers, students, community-based practitioners and participants in ACMI hands-on production workshops.

It celebrated the past, present and future of games and promoted this popular form of the moving image as a reflection of Australian culture.