Valcourt made the comment in response to criticisms from MP Niki Ashton, whose father Steve Ashton is a cabinet minister in the Manitoba government.
Manitoba has said it supports the Conservative bill, which aims to allow spouses living both on and off reserves the same rights to claim a share of the family's assets in the event of a marriage breakdown.
At committee hearings on the bill Tuesday, Ashton told Valcourt and Status of Women Minister Rona Ambrose to pay more attention to First Nations demands for a national inquiry into violence against aboriginal women.
"Maybe you should be listening to your father," Valcourt responded.
"The legislative assembly of Manitoba ....exhorted us to pass Bill S-2. If there is a province where there is an important aboriginal community, First Nations, who is experiencing serious issues and problems, it is Manitoba among others."
Ashton immediately responded that she was "offended" by Valcourt's reference to her father.
"If we're talking about paternalism, it takes many forms. Asking me who I talk to or don't talk to from my family is not part of what we're talking about in this committee."
Another Conservative MP rose to the minister's defence, but Valcourt quickly apologized.
"I want to be clear. I did not want to sound paternalistic. And if I have offended the member, I sincerely apologize. My point is simply this: we have been exhorted by the province of Manitoba and by others across Canada to give spouses on reserve the same rights that other Canadians enjoy."
His qualified apology comes less than a month after Valcourt apologized to NDP MP Romeo Saganash for questioning whether the noted Cree leader was of First Nations heritage.
In an interview, Ashton said she accepts the minister's apology. But she said the father-knows-best comments demonstrate not just the Conservatives' attitude towards her, but also towards the First Nations women who will be affected by the legislation at stake.
"Paternalism is alive and well amongst Harper Conservatives. We saw it in the attitude that came out today, but also in the bill that we're challenging," she said.
"One of our main arguments is that S-2 essentially, because of the lack of consultation, is paternalistic and ought to be opposed. They're telling us it's a way of ending violence against women, but that's not the case without the investments that need to be made."
Versions of the matrimonial real property bill have provoked tempers on all sides of the House since 2008. Critics say the government is being too paternalistic in designing the legislation, while the government says opposition parties are delaying crucial protections for aboriginal women.
"We've consulted for 25 years," Ambrose said. "Every day that goes by without passing this bill, these women are without protection."
The bill's genesis was in a 1986 Supreme Court ruling that said provincial laws on matrimonial rights did not apply to reserves, which are under federal jurisdiction. The federal government's bill is an attempt to fill that gap.
It would support First Nations in setting up their own legal regimes to determine a spouse's rights to the family home, and also give victimized spouses access to protections and immediate emergency services.
But the NDP and some First Nations leaders say they are concerned about the ability of reserves to actively and thoroughly implement the new regime.
They also say the legislation misses the point about victimization of women on reserves, which they argue is more related to poverty, high crime rates and crowded housing than it is to property rights.
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