Bernard Valcourt, who served in the Conservative cabinet of Brian Mulroney in the late 1980s and early 1990s, assumes the job with the clock ticking on a government promise to address long-standing and intractable treaty and land-claim issues.
The New Brunswick MP steps into the void left when John Duncan suddenly resigned last week after improperly writing to a tax court on behalf of a constituent.
Valcourt, 61, said in a release Friday he accepted the full cabinet post "with humility" and thanked Harper "for placing his confidence in me on this most important file."
Valcourt — who served as the secretary of state for Indian Affairs under Mulroney from 1987 to 1989 — will need to reacquaint himself with the file in a hurry.
More than a year ago, Harper met with aboriginal leaders in a highly symbolic summit that promised to reset the Crown-First Nations relationship.
Early last month, with national demonstrations by the Idle No More movement leaving the relationship in tatters, Harper and Duncan sat down again with national chiefs and committed to a new urgency in revisiting treaties and speeding up land-claim negotiations.
Duncan emerged to say that Harper and his bureaucratic backstop, the powerful Privy Council Office, would be taking an active role on "those sticky items which are identified which could use some direction from the centre."
There was talk of a second meeting taking place before the end of January.
However, internal First Nations political divisions, a health issue with Assembly of First Nations National Chief Shawn Atleo and Duncan's unexpected resignation have all conspired to undermine the appearance of progress.
Sources on both sides of the table maintain that talks are continuing, with the aim of scheduling the next, high-profile meeting when there is tangible progress to report.
Harper and Atleo are expected to meet again in coming weeks, with pressure mounting on Ottawa to put serious money for aboriginal education in the 2013 budget.
"This cabinet change comes at a unique time for First Nations and Canada, a true moment of reckoning where we have a commitment from the highest levels of the government of Canada to achieve real progress and transformative change for First Nations citizens," Atleo said in a release.
"We hope that Minister Valcourt will work with the First Nation leadership directly to advance priority areas to achieve transformative change for our peoples."
Valcourt appeared to promise as much.
"This January, the government committed itself to a high-level dialogue on the treaty relationship and comprehensive claims," Valcourt said Friday in a release.
"I am firmly of the view that working together is the best way to achieve our shared objective of healthier, more prosperous and self-sufficient aboriginal communities."
He said he looked forward to meeting with First Nations leaders "in the weeks and months to come."
Jean Crowder, the NDP aboriginal affairs critic, cited Valcourt's comments about working collaboratively, noting "that hasn't been the experience of the Harper government ... so it's going to be interesting to see whether he's able to change the channel."
Nonetheless, the New Democrat echoed the sentiments of many: "I think it's a good thing he's had cabinet experience and he's a very experienced politician."
The fractious regionalism and entrenched problems of the portfolio were immediately evident in the greeting Valcourt received Friday from Derek Nepinak, the outspoken head of the Assembly of Manitoba Chiefs.
Nepinak issued a release that stated the "development of the Canadian idea is also fundamentally different in western Canada because of treaties that opened the west to immigrant settlement."
"I am uncertain as to whether the minister from eastern Canada can or will fully understand the fundamental differences."
But Valcourt, a "red Tory" who grew up in the francophone, pulp-and-paper town of St. Quentin, N.B., got some stout regional backing from Roger Augustine, the AFN regional chief for New Brunswick and P.E.I.
"If the western guys give him a little bit of time, and educate him ... I can almost guarantee you that Derek Nepinak is going to be very happy with Bernard Valcourt," Augustine said in an interview.
Augustine said he's worked with Valcourt on a native regional economic development board.
"He's a street fighter," said the chief. "He's not afraid to go into a (tough) situation to help out."
"We're pretty anxious to get to work with him," added Augustine. "I just had a chat with the national chief (Atleo) and he's anxious to sit down and educate Bernard in every way, shape and form."
Duncan's resignation and Valcourt's promotion prompted a minor cabinet shuffle, with Veterans Affairs Minister Stephen Blaney taking on the Francophonie and Revenue Minister Gail Shea adding responsibility for the Atlantic Canada Opportunities Agency.
Kerry-Lynne Findlay, a B.C. MP, was promoted from the backbench to associate defence minister.
For Valcourt, Friday's move marks just the latest resurrection for a politician with a bruising past.
Valcourt was only months into his first full cabinet post under Mulroney when he crashed his motorcycle while impaired in 1989. The accident cost him an eye and his job as minister of Consumer and Corporate Affairs.
He subsequently returned to cabinet — first as fisheries minister and then at employment and immigration — before losing his seat in the devastating Conservative electoral wipeout of 1993.
Valcourt became leader of the New Brunswick Progressive Conservatives in 1995 but suffered another hard loss — winning just six seats — later that year in the provincial election. In 1997 he was replaced as the provincial party leader.
In 2011 he made a successful return to federal politics, winning the riding of Madawaska-Resigouche. Harper immediately made him a secretary of state — a junior cabinet minister — with the portfolios of ACOA and the Francophonie. Last July, Valcourt was given added duties as the associate minister of defence, a clear signal he was impressing the boss.
Friday's cabinet moves precede what many anticipate will be a more significant front-bench shake-up later this year as Harper positions his Conservatives — after more than seven years in government — for the 2015 election campaign.