diff --git a/ingest/ledgerbackend/testdata/sample-appendix-in-memory.cfg b/ingest/ledgerbackend/testdata/sample-appendix-in-memory.cfg
new file mode 100644
index 0000000000..958019998c
--- /dev/null
+++ b/ingest/ledgerbackend/testdata/sample-appendix-in-memory.cfg
@@ -0,0 +1,11 @@
+DEPRECATED_SQL_LEDGER_STATE = false
+
+[[HOME_DOMAINS]]
+HOME_DOMAIN="testnet.stellar.org"
+QUALITY="MEDIUM"
+
+[[VALIDATORS]]
+NAME="sdf_testnet_1"
+HOME_DOMAIN="testnet.stellar.org"
+PUBLIC_KEY="GDKXE2OZMJIPOSLNA6N6F2BVCI3O777I2OOC4BV7VOYUEHYX7RTRYA7Y"
+ADDRESS="localhost:123"
diff --git a/ingest/ledgerbackend/testdata/sample-appendix-deprecated_sql_ledger_state.cfg b/ingest/ledgerbackend/testdata/sample-appendix-on-disk.cfg
similarity index 100%
rename from ingest/ledgerbackend/testdata/sample-appendix-deprecated_sql_ledger_state.cfg
rename to ingest/ledgerbackend/testdata/sample-appendix-on-disk.cfg
diff --git a/ingest/ledgerbackend/toml.go b/ingest/ledgerbackend/toml.go
index efd2bdf3a9..1edb79f7db 100644
--- a/ingest/ledgerbackend/toml.go
+++ b/ingest/ledgerbackend/toml.go
@@ -24,7 +24,7 @@ var (
 	//go:embed configs/captive-core-testnet.cfg
 	TestnetDefaultConfig []byte
 
-	DefaultBucketListDBPageSize uint = 12
+	defaultBucketListDBPageSize uint = 12
 )
 
 const (
@@ -544,7 +544,7 @@ func (c *CaptiveCoreToml) setDefaults(params CaptiveCoreTomlParams) {
 		deprecatedSqlLedgerState = true
 	} else {
 		if !c.tree.Has("BUCKETLIST_DB_INDEX_PAGE_SIZE_EXPONENT") {
-			c.BucketListDBPageSizeExp = &DefaultBucketListDBPageSize
+			c.BucketListDBPageSizeExp = &defaultBucketListDBPageSize
 		}
 	}
 	c.DeprecatedSqlLedgerState = &deprecatedSqlLedgerState
@@ -641,8 +641,14 @@ func (c *CaptiveCoreToml) validate(params CaptiveCoreTomlParams) error {
 		)
 	}
 
-	if def := c.tree.Has("DEPRECATED_SQL_LEDGER_STATE"); def && params.UseDB && *c.DeprecatedSqlLedgerState {
-		return fmt.Errorf("CAPTIVE_CORE_USE_DB parameter is set to true, indicating stellar-core on-disk mode, in which DEPRECATED_SQL_LEDGER_STATE must be set to false")
+	if c.tree.Has("DEPRECATED_SQL_LEDGER_STATE") {
+		if params.UseDB && *c.DeprecatedSqlLedgerState {
+			return fmt.Errorf("CAPTIVE_CORE_USE_DB parameter is set to true, indicating stellar-core on-disk mode," +
+				" in which DEPRECATED_SQL_LEDGER_STATE must be set to false")
+		} else if !params.UseDB && !*c.DeprecatedSqlLedgerState {
+			return fmt.Errorf("CAPTIVE_CORE_USE_DB parameter is set to false, indicating stellar-core in-memory mode," +
+				" in which DEPRECATED_SQL_LEDGER_STATE must be set to true")
+		}
 	}
 
 	homeDomainSet := map[string]HomeDomain{}
diff --git a/ingest/ledgerbackend/toml_test.go b/ingest/ledgerbackend/toml_test.go
index 1c51068c44..a76d2c01f6 100644
--- a/ingest/ledgerbackend/toml_test.go
+++ b/ingest/ledgerbackend/toml_test.go
@@ -28,6 +28,7 @@ func TestCaptiveCoreTomlValidation(t *testing.T) {
 		peerPort          *uint
 		logPath           *string
 		expectedError     string
+		inMemory          bool
 	}{
 		{
 			name:              "mismatching NETWORK_PASSPHRASE",
@@ -204,11 +205,18 @@ func TestCaptiveCoreTomlValidation(t *testing.T) {
 			expectedError: "could not unmarshal captive core toml: setting BUCKET_DIR_PATH is disallowed for Captive Core, use CAPTIVE_CORE_STORAGE_PATH instead",
 		},
 		{
-			name:       "invalid DEPRECATED_SQL_LEDGER_STATE",
-			appendPath: filepath.Join("testdata", "sample-appendix-deprecated_sql_ledger_state.cfg"),
+			name:       "invalid DEPRECATED_SQL_LEDGER_STATE on-disk",
+			appendPath: filepath.Join("testdata", "sample-appendix-on-disk.cfg"),
 			expectedError: "invalid captive core toml: CAPTIVE_CORE_USE_DB parameter is set to true, indicating " +
 				"stellar-core on-disk mode, in which DEPRECATED_SQL_LEDGER_STATE must be set to false",
 		},
+		{
+			name:       "invalid DEPRECATED_SQL_LEDGER_STATE in-memory",
+			appendPath: filepath.Join("testdata", "sample-appendix-in-memory.cfg"),
+			expectedError: "invalid captive core toml: CAPTIVE_CORE_USE_DB parameter is set to false, indicating " +
+				"stellar-core in-memory mode, in which DEPRECATED_SQL_LEDGER_STATE must be set to true",
+			inMemory: true,
+		},
 	} {
 		t.Run(testCase.name, func(t *testing.T) {
 			params := CaptiveCoreTomlParams{
@@ -218,7 +226,7 @@ func TestCaptiveCoreTomlValidation(t *testing.T) {
 				PeerPort:           testCase.peerPort,
 				LogPath:            testCase.logPath,
 				Strict:             true,
-				UseDB:              true,
+				UseDB:              !testCase.inMemory,
 			}
 			_, err := NewCaptiveCoreTomlFromFile(testCase.appendPath, params)
 			assert.EqualError(t, err, testCase.expectedError)
@@ -522,7 +530,7 @@ func TestDBConfigDefaultsToSqlite(t *testing.T) {
 	require.NoError(t, toml.unmarshal(configBytes, true))
 	assert.Equal(t, toml.Database, "sqlite3://stellar.db")
 	assert.Equal(t, *toml.DeprecatedSqlLedgerState, false)
-	assert.Equal(t, *toml.BucketListDBPageSizeExp, DefaultBucketListDBPageSize)
+	assert.Equal(t, *toml.BucketListDBPageSizeExp, defaultBucketListDBPageSize)
 	assert.Equal(t, toml.BucketListDBCutoff, (*uint)(nil))
 }