MI5, MI6 and GCHQ will hire applicants who have the "right mix of minds and skills" to tackle threats to the UK.
People could previously only apply to those agencies if one of their parents were classed as a British citizen - or had citizenship from an approved country.
New applicants must still be a British citizen despite the changes.
Officials say recruitment will continue to have a thorough vetting process, which will look at background, lifestyle and personal connections that will help respond to any risks.
A spokesperson, speaking on behalf of GCHQ, MI5 and MI6, said: "We perform best in our mission to keep the nation safe and further the UK's interests when we reflect the diversity of the country we serve.
"By recruiting people from the widest possible range of backgrounds, we can innovate, challenge established ways of thinking and welcome the very brightest and best people to join us.
"The parental nationality rule unnecessarily stopped brilliant people from applying to work with us.
"Removing this blanket rule means that all British citizens who apply for jobs in our agencies can now be assessed on their abilities and not where their parents are from."
The previous approved list of nationalities for applicants' parents included: British Overseas Territory, British Subject, British National (Overseas), British Overseas Citizen, British Protected Person, citizenship of a country of the Commonwealth, citizenship of a country in the European Economic Area (EEA), or citizenship of the US.
The three agencies recently launched an advert to find candidates for an 11-week summer diversity intelligence internship.
It aims to find candidates from black, Asian or minority ethnic backgrounds or people from a socially or economically disadvantaged background.
MI5 has also previously been recognised for its diversity efforts after being voted the UK's most gay-friendly employer by the Stonewall charity back in 2016.
At the time, MI5 director general Andrew Parker said: "Diversity is vital for MI5, not just because it's right that we represent the communities we serve, but because we rely on the skills of the most talented people whoever they are, and wherever they may be."