The charity says teachers should be at the heart of careers education with the support of policy makers and businesses.
It says pupils from disadvantaged backgrounds are particularly likely to lose out from poor careers guidance.
The proportion of poorer young people not in education, employment or training after the age of 16, is five times that of their wealthier classmates according to the charity's analysis of official figures.
It wants to see a teacher or member of middle management trained to take the lead on careers guidance in every school.
This would allow them to build and manage links with employers, businesses and independent careers experts and ensure children learn about the working world.
Jude Heaton, Teach First's director for higher education access and employability, said the need for better careers and employability education had "acute moral and economic implications for all of us".
"As those best placed to support children with their aspirations and careers choices, teachers are at the core of any lasting solution, yet too often when we talk about the paths in life that are right for young people, teachers are an afterthought. This needs to change."