The Padma Shri awardee, who was nicknamed 'The Flying Sikh' for his accomplishments, was 91 and is survived by his golfer son Jeev Milkha Singh and three daughters.
"It is with extreme sadness that we would like to inform you that Milkha Singh Ji passed away at 11.30 pm. on the 18th of June 2021," read a statement from the family.
"He fought hard but God has his ways and it was perhaps true love and companionship that both our mother Nirmal ji and now Dad have passed away in a matter of 5 days," it added.
His condition turned critical this evening as he developed complications, including fever and dipping oxygen saturation levels, after a bout with COVID-19, in the Intensive Care Unit of the PGIMER hospital in Chandigarh.
"We are deeply indebted to the doctors at PGI for their valiant efforts and the love and prayers we received from across the world and from yourselves," the family stated.
One of independent India's biggest sporting icons, ace sprinter Milkha Singh, died on Friday after a month-long battle with COVID-19, during which he lost his former national volleyball captain wife Nirmal Kaur to the same ailment.
The PGIMER also issued a statement and expressed its condolences.
"...despite best of the efforts by a medical team, Milkha Singh ji could not be retrieved from his critical condition and after a brave fight, he left for his heavenly abode at 11:30 pm," the hospital stated.
PGIMER Director Prof Jagat Ram said Milkha "will be remembered for his exceptional accomplishments on and off the field and his endearing and humane personality."
Milkha had contracted COVID-19 last month and tested negative for the virus on Wednesday when he was shifted to general ICU in another block of the hospital.
Milkha's 85-year-old wife Nirmal, who had also been infected by the virus, passed away at a private hospital in Mohali on Sunday. The couple were suspected to have contracted the infection from a house help.
Milkha was admitted to PGIMER on June 3 after his oxygen levels dipped at home following treatment at the Fortis hospital in Mohali for a week.
The legendary athlete is a four-time Asian Games gold medallist and the 1958 Commonwealth Games champion but his greatest performance remains the fourth-place finish in the 400m final of the 1960 Rome Olympics.
His timing of 45.6 sec at the Italian capital remained the national record for 38 years before Paramjeet Singh broke it in 1998.
He also represented India in the 1956 and 1964 Olympics and was bestowed the Padma Shri in 1959.
After testing positive for COVID-19 on May 19, Milkha had remained in home isolation at his Chandigarh residence till May 23 and was admitted to Fortis hospital in Mohali on May 24 as he kept running fever, had body aches and experienced loss of appetite.
His golfer son Jeev, who was in Dubai at that time, had reached Chandigarh on May 22 while another daughter Mona Milkha Singh, a doctor in the United States, also arrived later.
Fortis hospital had earlier diagnosed the couple with "COVID pneumonia".
While in Fortis, the couple also shared the same room for a few days.
After being admitted to PGIMER earlier this month, Milkha had received a phone call from Prime Minister Narendra Modi, enquiring about his health.
Modi, while condoling Milkha's demise, remembered that conversation on Friday and said that "little did I know that it would be our last conversation."
"In the passing away of Shri Milkha Singh Ji, we have lost a colossal sportsperson, who captured the nation's imagination and had a special place in the hearts of countless Indians.
"His inspiring personality endeared himself to millions. Anguished by his passing away," the Prime Minister tweeted.