The additional capacity would encourage competition between airlines and bring down prices for Scottish passengers, UK aviation minister Baroness Sugg said on a visit to Glasgow Airport.
It came as international trade minister and runway opponent Greg Hands quit after it was confirmed Conservative MPs will not be given a free vote on the issue.
Campaigners from the No 3rd Runway Coalition today urged the SNP to reverse its support for the scheme with a demonstration at Holyrood.
Baroness Sugg confirmed the UK Government will act if required to reserve around 15 per cent of new slots at Heathrow for domestic flights which would guarantee connections with Scotland.
Public Service Obligations (PSOs), which already exist to protect flights from one city to another, would be put in place to protect routes if required.
It could also make flights cheaper, with these PSOs being exempt from Air Passenger Duty - currently £26 per passenger for return flights within the UK.
The minister said it could lead to new Scottish routes from Heathrow, referring to Flybe’s interest in a service from Dundee.
She said the new Scottish slots would be at “helpful and sensible times” to prevent cross-Border flights at busy times being squeezed out by other routes.
The third runway issue has proved controversial south of the Border but Baroness Sugg believes the proposals, which will be voted on by MPs on Monday, have support across Scotland.
She said: “I’ve just been meeting with Scottish business people who are hugely supportive, and obviously Glasgow Airport who are too.
“I think we’ve got great cross-party political support with the SNP being clear (in support) but it’s going to be down to the Scottish MPs voting on Monday, and we really want to make sure that they do vote for Heathrow because it has taken a while, we are keen to get on with it and we think it will really benefit Scotland.
“What we’ve seen in recent years is domestic flights squeezed out of Heathrow because there is so much demand there, so if we don’t have an expanded Heathrow then we are going to see more of that, so there is a cost to not expanding too.”
But Rob Barnstone of the No 3rd Runway Coalition, said: “Plans to expand Heathrow will be to the detriment of Scotland.
“It puts at risk the Scottish Government’s own tough climate change targets, which would be impossible to achieve with Heathrow expansion.
“Expansion at Heathrow will also impact Scottish airports, as any growth will be routed through London and not direct to international markets that could instead be served.”
Derek Provan, chief executive of AGS airports, which owns Aberdeen, Glasgow and Southampton airports, said increased Heathrow links are “imperative for Scottish business”.
He said: “As an example, Glasgow has ten flights a day and Aberdeen seven to London and they are full most days, and 40 per cent of those passengers are connecting through London somewhere else globally that we’re unable to support with a direct route.
“This opportunity that allows us to have effectively ring-fenced extra flights from Scotland to London is imperative for Scottish business.”
Flybe and easyJet have already outlined new routes they would expect to serve from an expanded Heathrow, with extra competition on existing routes potentially lowering fares by up to 30 per cent, the UK Government claimed.
Mr Hands said he was standing down to honour a pledge to his west London constituents to oppose expansion of the airport.
His decision again throws the spotlight onto Foreign Secretary Boris Johnson, who has been a long-standing and vocal opponent of the runway.
A UK Government source said Mr Johnson will be “out of the country” on Monday but refused to reveal where “due to security reasons”.
The Commons vote coincides with a meeting of EU foreign ministers in Luxembourg, but Foreign Office Minister Sir Alan Duncan is expected to attend rather than Mr Johnson.