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
362 Cedarstone Way, St. Augustine

$755,000

362 Cedarstone Way, St. Augustine

4 Beds 4 Baths 2,796 SqFt Residential MLS® # 2113036
New
7750 Wyndwood Drive, St. Johns

$490,000

7750 Wyndwood Drive, St. Johns

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

$805,000

3732 Berenstain Drive, St. Augustine

4 Beds 3 Baths 2,914 SqFt Residential MLS® # 2111704
301 S Roscoe Boulevard, Ponte Vedra Beach

$6,950,000

301 S Roscoe Boulevard, Ponte Vedra Beach

6 Beds 7 Baths 5,734 SqFt Residential MLS® # 2084500
119 Lily Landing Drive, St. Augustine

$699,000

119 Lily Landing Drive, St. Augustine

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

$1,555,000

↓ $40,000

301 Courtney Oaks Drive, St. Augustine

5 Beds 5 Baths 4,250 SqFt Residential MLS® # 2109813
1774 Wildwood Drive, St. Augustine

$599,000

1774 Wildwood Drive, St. Augustine

5 Beds 2 Baths 2,472 SqFt Residential MLS® # 2109485
432 Aj Mills Road, Ponte Vedra

$3,300,000

432 Aj Mills Road, Ponte Vedra

6 Beds 8 Baths 6,711 SqFt Residential MLS® # 2108924
Under Contract
403 Rio Del Norte Road, St. Augustine

$925,000

↓ $75,000

403 Rio Del Norte Road, St. Augustine

4 Beds 3 Baths 2,536 SqFt Residential MLS® # 2107543
252 Bermuda Greens Avenue, Ponte Vedra

$1,750,000

252 Bermuda Greens Avenue, Ponte Vedra

5 Beds 6 Baths 5,081 SqFt Residential MLS® # 2107632
123 Thatcham Drive, St. Augustine

$579,999

123 Thatcham Drive, St. Augustine

3 Beds 3 Baths 2,361 SqFt Residential MLS® # 2108277
1625 Masters Drive, St. Augustine

$311,000

1625 Masters Drive, St. Augustine

4 Beds 3 Baths 1,973 SqFt Residential MLS® # 2083731
Under Contract
638 Windley Drive, St. Augustine

$850,000

↓ $19,000

638 Windley Drive, St. Augustine

5 Beds 5 Baths 4,031 SqFt Residential MLS® # 2107339
Under Contract
1231 Neck Road, Ponte Vedra Beach

$2,750,000

1231 Neck Road, Ponte Vedra Beach

4 Beds 5 Baths 4,157 SqFt Residential MLS® # 2107271
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
535 Crescent Key Drive, St. Augustine

$585,000

↓ $14,000

535 Crescent Key Drive, St. Augustine

4 Beds 4 Baths 2,792 SqFt Residential MLS® # 2106192
Under Contract
129 Bear Point, Ponte Vedra

$2,600,000

↓ $350,000

129 Bear Point, Ponte Vedra

4 Beds 5 Baths 4,666 SqFt Residential MLS® # 2104207
27 Deer Meadows Drive, St. Augustine

$545,000

↓ $5,000

27 Deer Meadows Drive, St. Augustine

5 Beds 4 Baths 2,864 SqFt Residential MLS® # 2101855
Under Contract
66 Magdaleno Court, St. Augustine

$785,000

66 Magdaleno Court, St. Augustine

5 Beds 4 Baths 3,661 SqFt Residential MLS® # 2102769
Pending
10 Firefly Trace, St. Augustine

$675,000

↓ $10,000

10 Firefly Trace, St. Augustine

5 Beds 4 Baths 3,396 SqFt Residential MLS® # 2100464
184 Whistling Run, St. Augustine

$649,000

↓ $11,000

184 Whistling Run, St. Augustine

4 Beds 4 Baths 3,147 SqFt Residential MLS® # 2097813
772 Blind Oak Circle, St. Augustine

$925,000

772 Blind Oak Circle, St. Augustine

5 Beds 5 Baths 4,284 SqFt Residential MLS® # 2099513
363 Latrobe Avenue, St. Augustine

$765,000

↓ $33,000

363 Latrobe Avenue, St. Augustine

5 Beds 4 Baths 3,165 SqFt Residential MLS® # 2098730

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

St. John's County Multi-Generational Homes housing market statistics: As of October 14, 2025 there are currently 43 properties for sale in St. John's County Multi-Generational Homes, with an average asking price of $1,476,217. The highest-priced property is $6,950,000 and the lowest-priced property can be purchased for $311,000. St. John's County Multi-Generational Homes listings have an average price of $362 per square feet, based on listings with 5 beds, 4 baths, and 3,694 square feet of living space.