And it could see an increase of 30,000 residents living in the district.
Up to 9,185 new homes are expected to be built in south Lancaster over the next 25 years, many of them as part of a new Bailrigg Garden Village.
Last year the government approved £140m in funding for south Lancaster as part of an overall £261.2m estimated cost of the work to be carried out.
The successful bid by Lancashire County Council means Housing Infrastructure Fund (HIF) cash will help deliver a reconfigured M6 junction 33 as well as a new 2.5km highway connection running north parallel to the M6 from junction 33 to connect south Lancaster directly to the current road network, bypassing Galgate.
The new connection would link into an improved Hazelrigg Lane, immediately to the south of Lancaster University
A new 2km spine road would also be built, opening up greenfield land for the development of Bailrigg Garden Village and including a new road underpass of the West Coast Main Line.
This would tie in with a new bridge across Lancaster Canal.
However, despite the £140m government funding, and an estimated £98m in developer contributions, the remaining £23.2m would need to be found towards improved public transport and cycle links (including a significant remodelling of the city centre one-way system), new primary and secondary schools and new GP provision for the area.
Funding would also be needed to bridge the gap between the infrastructure being developed and the payment of developer contributions, which would likely be spread over 25 years.
"There are a lot of questions to be asked about what happens if [£261.2m] isn't the final figure," Coun Jackson said.
A discussion is due to be held on the issue at tonight's full council meeting to ensure all councillors were fully aware of the subject.
A final decision could then be made at full council on July 28, when a partnership agreement is expected to be agreed on how the city and county councils will move forward to deliver and pay for the infrastructure.
If all goes ahead, some housing could be ready by 2023, with the road restructuring completed by 2027.
Ahead of today's meeting, Coun Jackson said the decisions to be made over the next few months would be crucial for everyone living in the district.
"It's going to be the biggest decision this council has made in probably 20 or 30 years," she said. "It's quite a challenge for everyone to absorb it and understand the consequences for us as a city.
"It will make a massive difference over the next 25 years. There's nobody who won't be affected by this decision.
"But the question is, how do we create the smaller more manageable development Lancaster really needs and what is the wisest thing to do about our transport network?"
Coun Jackson said there were concerns over plans for 9,185 new homes in south Lancaster as a whole, including around 5,000 within the garden village scheme - a figure which has already raised some concerns.
This could potentially see around 30,000 new residents in a city which currently has a population of around 53,000 - within a district of 148,000 - which Coun Jackson said would naturally lead to a vast increase in car movements.
"The size of the final development is far larger than we originally expected," Coun Jackson said.
"It would take some time to set up the necessary infrastructure for a development of that size."
In such a large amount of housing, the council would also wish to see a sizeable amount of affordable housing - potentially around 30 per cent of the final figure.
Coun Tim Hamilton-Cox, cabinet member with responsibility for sustainable economic prosperity, said a further concern was the risk involved with such a financial model.
With a developer contribution of £98m spread over 25 years there would need to be up front borrowing to pay for the infrastructure, with the financial modelling assuming that Lancashire County Council would have to raise this finance.
To further complicate matters, any county council debt would have to be taken on by a new Bay authority if that is approved later this year.
Council officers are recommending that councillors approve a non-legally binding principles agreement when they meet this evening, ahead of a final decision being made next month.
They say the infrastructure investment would deliver the Bailrigg Garden Village project and create new places and neighbourhoods "for the benefit of people and communities in south Lancaster".
And in their report to council they say there are "no economic disadvantages in delivering the South Lancaster Growth Catalyst Programme", and say a failure to enter into a principles agreement with Lancashire County Council "will result in reputational damage to Lancaster City Council" as it is unlikely that the government funding will be allocated and there are "potential wider strategic implications" that could be affected by such a decision.