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 Open House
383 Pine Haven Drive, St. Johns

$935,000

383 Pine Haven Drive, St. Johns

5 Beds 5 Baths 3,597 SqFt Residential
Sat, Sep 12th, 2026 @ 11am - 1pm
MLS® # 2163437
704 Coachman's Place, St. Augustine

$999,000

704 Coachman's Place, St. Augustine

5 Beds 4 Baths 2,993 SqFt Residential MLS® # 2162645
3530 Datura Street, St. Augustine

$599,000

3530 Datura Street, St. Augustine

6 Beds 7 Baths 1,893 SqFt Residential MLS® # 2162502
448 Old Hickory Forest Road, St. Augustine

$690,000

448 Old Hickory Forest Road, St. Augustine

4 Beds 3 Baths 2,645 SqFt Residential MLS® # 2162473
9151 June Lane, St. Augustine

$1,490,000

9151 June Lane, St. Augustine

3 Beds 3 Baths 2,854 SqFt Residential MLS® # 2162354
3120 S Cassata Lane, St. Augustine

$640,000

3120 S Cassata Lane, St. Augustine

6 Beds 4 Baths 3,029 SqFt Residential MLS® # 2162219
1101 Roundtree Circle, St. Johns

$520,000

1101 Roundtree Circle, St. Johns

6 Beds 4 Baths 3,502 SqFt Residential MLS® # 2156941
New
305 Sternwheel Drive, St. Johns

$750,000

305 Sternwheel Drive, St. Johns

5 Beds 4 Baths 3,148 SqFt Residential MLS® # 2161848
Under Contract
105 Bloomfield Way, St. Augustine

$474,900

105 Bloomfield Way, St. Augustine

4 Beds 4 Baths 2,270 SqFt Residential MLS® # 2161778
Open House
308 Rustic Mill Drive, St. Augustine

$560,000

308 Rustic Mill Drive, St. Augustine

2 Beds 3 Baths 2,564 SqFt Residential
Sat, Sep 12th, 2026 @ 11am - 1pm
MLS® # 2160756
Under Contract
103 Sitara Lane, Fruit Cove

$1,300,000

103 Sitara Lane, Fruit Cove

6 Beds 7 Baths 5,791 SqFt Residential MLS® # 2159422
Pending
157 Lawn Avenue, St. Augustine

$1,400,000

157 Lawn Avenue, St. Augustine

7 Beds 5 Baths 4,100 SqFt Residential MLS® # 2159371
309 S Forest Dune Drive, St. Augustine

$2,250,000

309 S Forest Dune Drive, St. Augustine

5 Beds 5 Baths 4,480 SqFt Residential MLS® # 2158674
50 Sandy Palm Trail, St. Augustine

$549,900

50 Sandy Palm Trail, St. Augustine

5 Beds 5 Baths 3,266 SqFt Residential MLS® # 2158278
Under Contract
255 Split Oak Road, St. Augustine

$638,000

255 Split Oak Road, St. Augustine

4 Beds 4 Baths 2,800 SqFt Residential MLS® # 2157575
63 Golden Fern Drive, St. Augustine

$647,500

↓ $2,400

63 Golden Fern Drive, St. Augustine

4 Beds 4 Baths 2,952 SqFt Residential MLS® # 2156738
13 Rohde Avenue, St. Augustine

$1,499,000

13 Rohde Avenue, St. Augustine

7 Beds 5 Baths 3,214 SqFt Residential MLS® # 2155822
Under Contract
58 Blue Hampton Drive, Ponte Vedra

$845,500

↓ $69,500

58 Blue Hampton Drive, Ponte Vedra

4 Beds 4 Baths 2,958 SqFt Residential MLS® # 2153338
4710 State Road 13 N, St. Johns

$4,900,000

4710 State Road 13 N, St. Johns

9 Beds 10 Baths 7,603 SqFt Residential MLS® # 2152645
144 Plantation Circle S, Ponte Vedra Beach

$5,900,000

144 Plantation Circle S, Ponte Vedra Beach

5 Beds 9 Baths 8,301 SqFt Residential MLS® # 2151550
Under Contract
828 Riley Lane, St. Augustine

$810,000

828 Riley Lane, St. Augustine

5 Beds 3 Baths 3,083 SqFt Residential MLS® # 2151484
250 Shadow Cove, St. Johns

$873,000

↓ $27,000

250 Shadow Cove, St. Johns

5 Beds 4 Baths 3,245 SqFt Residential MLS® # 2145950
121 Carriage Lamp Way, Ponte Vedra Beach

$2,500,000

121 Carriage Lamp Way, Ponte Vedra Beach

5 Beds 6 Baths 4,677 SqFt Residential MLS® # 2145712
323 Aspinwall Parkway, St. Augustine

$999,000

↓ $51,000

323 Aspinwall Parkway, St. Augustine

5 Beds 4 Baths 3,718 SqFt Residential MLS® # 2150197

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

St. John's County Multi-Generational Homes housing market statistics: As of September 8, 2026 there are currently 41 properties for sale in St. John's County Multi-Generational Homes, with an average asking price of $1,415,166. The highest-priced property is $5,900,000 and the lowest-priced property can be purchased for $380,000. St. John's County Multi-Generational Homes listings have an average price of $367 per square feet, based on listings with 5 beds, 5 baths, and 3,626 square feet of living space.