Andrew Hunter, the Art Gallery of Ontario’s top curator of Canadian art, resigned Thursday, according to an internal memo, and it’s hard to see it as anything less than a blow to the gallery’s progressive arc of recent years.

The gallery confirmed Hunter’s departure Thursday afternoon. Hunter, reached on the phone, said that his resignation was not with a specific destination in mind. “I’ve always made my career decisions based on ideas, around community, and around family,” he said. “Maybe that’s a flaw — I’ve never really managed my career as a career. I always gravitate to where I feel I belong.”

Nonetheless, the timing seems a little strange, with Hunter coming off his most triumphant exhibition, Every. Now. Then., a powerfully inclusive, unblinkingly critical take on contemporary Canadian nationhood.

The show stands as a high-water mark for the ambitions of any museum grappling with keeping a bead on a rapidly splintering society and audience: It refutes master narratives in favour of hidden histories — driven whether by race, gender, or economic disparity — and unflinchingly demands that we, as Canadians, face the reality of our country, past and present, unpleasant though it may be.

In a blithely celebratory moment of Canada 150, it provided a necessary drop of poison in the public ear. More importantly, it pried open wide the institution’s doors to artists and communities it had historically kept at bay. It said, in no uncertain terms, that a museum cannot function apart from the messy social context in which it dwells, but rather must do so because of it.

In a statement, AGO director Stephan Jost praised Hunter’s work at the gallery and singled out Every. Now. Then. specifically: “Andrew has helped us think more critically, deeply and compassionately about our country and our world — and he has made an incredible difference at the Gallery as a result.”

Hunter said that the show’s deep dive into grassroots and community arts initiatives helped reawaken his own commitment to those worlds, and spurred his decision to leave. “I feel like it pointed me more clearly in a direction I was already heading,” he said. A recent Aboriginal youth workshop Hunter attended in northern Ontario this summer solidified the urge. “It really reminded me of what’s important to me.”

It many ways, Every. Now. Then. expressed the apex of Hunter’s ambition, which I suppose makes it a high note on which to go out. At the same time, if it signals the end to Hunter’s project, the gallery is in some trouble. Hunter was hired in 2013 as an outlier. Coming from outside the institutional system with a background in independent curating, community arts and experimental social practice (Dodolab, which he co-founded with Lisa Hirmer in 2009, and Hirmer still runs, was a crucible of these concerns), Hunter was the least conventional hire the AGO could make.

In other words, he was exactly what it needed. Coming out of its long Frank Gehry renovation in 2009, the gallery capped its transformation with an ill-advised, out-of-the-box imported blockbuster with King Tut: The Boy King. That piqued local anxieties as to the “new” AGO’s ambitions, leaving most to fret that the gallery would further detach from its time and place to play in some kind of generically “global” context.

Then-director Matthew Teitelbaum bore the brunt of those anxieties personally, and slowly turned the ship towards a core priority of balance, intertwining the gallery’s international ambitions with the critical foundation of its here and now. The AGO smartened up, crafting such things as long-overdue surveys of senior Toronto-based artists Suzy Lake and Stephen Andrews, and even in its blockbuster offerings never forgot the city outside its walls.

Hunter’s appointment by Teitelbaum deepened that commitment in an outward way. Teitelbaum had reset course, and appointed Hunter to maintain it. He pushed hard against convention, even in the most conventional tasks: A retrospective of Alex Colville, inflected by filmmakers Wes Anderson and the Coen Brothers, or the epic Hollywoodization of Lawren Harris, as curated by Steve Martin, which Hunter brought home and de-sanitized from its high-Modern purity, connecting it with the hardscrabble realities of early industrial-era Toronto, roiling with inequity.

Hunter has been a leader in eroding traditional barriers, demanding marginalized histories take their rightful place alongside official versions. He championed Indigenous art, overseeing a reinstallation of the museum’s permanent Canadian collection that wove Indigenous art into the traditional display. He refused to see divisions between sectors of the art world siloed by haughty convention, and happily surrendered authority to voices unaccustomed to taking the lead.

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He led the way in establishing the museum’s first curator of Indigenous art, Wanda Nanibush (her current exhibition is a retrospective of iconic Indigenous Toronto-based painter Rita Letendre) and has gamely collaborated wherever possible — most recently for Every. Now. Then. with Anique Jordan, an African-Canadian independent curator.

In other words, Hunter’s mission was to make the AGO relevant to the world outside its doors in a deep and real way. For maybe the first time in its history, it is. The gallery’s task now, with two key positions now vacant — Hunter’s, and the role of chief curator — is to decide whether to maintain course, or chart a new direction. It does the latter at its peril.