St. John's County Homes With Mother In-Law Suite

Looking for a home with a mother in-law suite in St. John's County, FL. Featured here are all St. John's County Multi-Generational homes for sale and St. John's County Multi-Generational real estate. If you’re interested in any of the St. John's County Multi-Generational home listings that you see below, just click the "Ask a Question" button when viewing the details of that property. Our St. John's County real estate agents can provide you with disclosures, past sales history, dates and prices of properties recently sold nearby, and other details related to the St. John's County Multi-Generational home home market.

And if you're interested in St. John's County Multi-Generational homes for sale, we also invite you to register for a free account so that you can receive email alerts whenever new homes with a mother in-law suite in St. John's County hit the market, allowing you to stay one-step ahead of other buyers in the area. And remember to call or text us directly with any additional questions you have about buying or selling a home in St. John's County, Florida. 

St. John's County Multi-Generational Homes For Sale

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New Pending
363 Latrobe Avenue, St. Augustine

$765,000

363 Latrobe Avenue, St. Augustine

5 Beds 4 Baths 3,165 SqFt Residential MLS® # 2098730
New Under Contract
4708 State Rd 13 N, St. Johns

$3,000,000

4708 State Rd 13 N, St. Johns

5 Beds 5 Baths 5,382 SqFt Residential MLS® # 2125476
New
100 Coppinger Place, St. Johns

$850,000

100 Coppinger Place, St. Johns

5 Beds 4 Baths 3,036 SqFt Residential MLS® # 2125295
Under Contract
30 Franklin Avenue, Ponte Vedra Beach

$2,500,000

30 Franklin Avenue, Ponte Vedra Beach

4 Beds 5 Baths 3,800 SqFt Residential MLS® # 2123588
13900 County Rd 13 N, St. Augustine

$1,325,000

13900 County Rd 13 N, St. Augustine

3 Beds 3 Baths 2,166 SqFt Residential MLS® # 2123899
772 Blind Oak Circle, St. Augustine

$899,000

772 Blind Oak Circle, St. Augustine

5 Beds 5 Baths 4,284 SqFt Residential MLS® # 2123573
178 Antolin Way, St. Augustine

$1,250,000

↓ $70,000

178 Antolin Way, St. Augustine

6 Beds 5 Baths 3,728 SqFt Residential MLS® # 2121355
6698 A1a S, St. Augustine

$765,000

6698 A1a S, St. Augustine

4 Beds 4 Baths 3,416 SqFt Residential MLS® # 2120590
301 Roscoe Boulevard S, Ponte Vedra Beach

$6,750,000

301 Roscoe Boulevard S, Ponte Vedra Beach

4 Beds 7 Baths 5,734 SqFt Residential MLS® # 2120512
2624 Oakgrove Avenue, St. Augustine

$1,525,000

↓ $59,999

2624 Oakgrove Avenue, St. Augustine

5 Beds 7 Baths 5,083 SqFt Residential MLS® # 2088093
644 Sand Isles Circle, Ponte Vedra Beach

$895,000

644 Sand Isles Circle, Ponte Vedra Beach

4 Beds 3 Baths 2,217 SqFt Residential MLS® # 2118529
153 Washington Street, St. Augustine

$2,150,000

153 Washington Street, St. Augustine

3 Beds 4 Baths 2,489 SqFt Residential MLS® # 2118038
535 Hedgewood Drive, St. Augustine

$399,900

535 Hedgewood Drive, St. Augustine

3 Beds 4 Baths 2,147 SqFt Residential MLS® # 2117155
Under Contract
35 Townsend Place, St. Augustine

$2,690,000

35 Townsend Place, St. Augustine

8 Beds 11 Baths 6,636 SqFt Residential MLS® # 2116449
2878 Adams Road, St. Augustine

$1,389,000

2878 Adams Road, St. Augustine

3 Beds 3 Baths 3,071 SqFt Residential MLS® # 2115668
7750 Wyndwood Drive, St. Johns

$470,000

↓ $5,000

7750 Wyndwood Drive, St. Johns

3 Beds 3 Baths 1,375 SqFt Residential MLS® # 2112787
3732 Berenstain Drive, St. Augustine

$745,000

↓ $5,000

3732 Berenstain Drive, St. Augustine

4 Beds 3 Baths 2,914 SqFt Residential MLS® # 2111704
119 Lily Landing Drive, St. Augustine

$679,000

↓ $20,000

119 Lily Landing Drive, St. Augustine

5 Beds 4 Baths 2,996 SqFt Residential MLS® # 2110963
Under Contract
301 Courtney Oaks Drive, St. Augustine

$1,499,999

↓ $55,001

301 Courtney Oaks Drive, St. Augustine

5 Beds 5 Baths 4,250 SqFt Residential MLS® # 2109813
432 Aj Mills Road, Ponte Vedra

$3,200,000

↓ $100,000

432 Aj Mills Road, Ponte Vedra

6 Beds 8 Baths 6,711 SqFt Residential MLS® # 2108924
252 Bermuda Greens Avenue, Ponte Vedra

$1,679,000

↓ $71,000

252 Bermuda Greens Avenue, Ponte Vedra

5 Beds 6 Baths 5,081 SqFt Residential MLS® # 2107632
842 Fruit Cove Road, St. Johns

$4,075,000

842 Fruit Cove Road, St. Johns

3 Beds 4 Baths 5,119 SqFt Residential MLS® # 2105895
8225 Hardwood Landing Road, St. Augustine

$1,159,000

8225 Hardwood Landing Road, St. Augustine

3 Beds 4 Baths 3,322 SqFt Residential MLS® # 2106861
6721 Veronica Court, St. Augustine

$950,000

↓ $49,000

6721 Veronica Court, St. Augustine

10 Beds 6 Baths 5,132 SqFt Residential MLS® # 2096285

St. John's County Multi-Generational Homes Market Stats

St. John's County Multi-Generational Homes housing market statistics: As of January 21, 2026 there are currently 28 properties for sale in St. John's County Multi-Generational Homes, with an average asking price of $1,813,264. The highest-priced property is $6,750,000 and the lowest-priced property can be purchased for $399,900. St. John's County Multi-Generational Homes listings have an average price of $430 per square feet, based on listings with 5 beds, 5 baths, and 3,941 square feet of living space.