diff --git a/internal/rukpak/convert/registryv1.go b/internal/rukpak/convert/registryv1.go
index e2eff3bc3..c26d16161 100644
--- a/internal/rukpak/convert/registryv1.go
+++ b/internal/rukpak/convert/registryv1.go
@@ -4,6 +4,7 @@ import (
 	"context"
 	"crypto/sha256"
 	"encoding/json"
+	"errors"
 	"fmt"
 	"io/fs"
 	"path/filepath"
@@ -23,6 +24,7 @@ import (
 	"sigs.k8s.io/yaml"
 
 	"github.com/operator-framework/api/pkg/operators/v1alpha1"
+	"github.com/operator-framework/operator-registry/alpha/property"
 	registrybundle "github.com/operator-framework/operator-registry/pkg/lib/bundle"
 
 	registry "github.com/operator-framework/operator-controller/internal/rukpak/operator-registry"
@@ -43,12 +45,12 @@ func RegistryV1ToHelmChart(ctx context.Context, rv1 fs.FS, installNamespace stri
 	l := log.FromContext(ctx)
 
 	reg := RegistryV1{}
-	fileData, err := fs.ReadFile(rv1, filepath.Join("metadata", "annotations.yaml"))
+	annotationsFileData, err := fs.ReadFile(rv1, filepath.Join("metadata", "annotations.yaml"))
 	if err != nil {
 		return nil, err
 	}
 	annotationsFile := registry.AnnotationsFile{}
-	if err := yaml.Unmarshal(fileData, &annotationsFile); err != nil {
+	if err := yaml.Unmarshal(annotationsFileData, &annotationsFile); err != nil {
 		return nil, err
 	}
 	reg.PackageName = annotationsFile.Annotations.PackageName
@@ -101,9 +103,61 @@ func RegistryV1ToHelmChart(ctx context.Context, rv1 fs.FS, installNamespace stri
 		return nil, err
 	}
 
+	if err := copyMetadataPropertiesToCSV(&reg.CSV, rv1); err != nil {
+		return nil, err
+	}
+
 	return toChart(reg, installNamespace, watchNamespaces)
 }
 
+// copyMetadataPropertiesToCSV copies properties from `metadata/propeties.yaml` (in the filesystem fsys) into
+// the CSV's `.metadata.annotations['olm.properties']` value, preserving any properties that are already
+// present in the annotations.
+func copyMetadataPropertiesToCSV(csv *v1alpha1.ClusterServiceVersion, fsys fs.FS) error {
+	var allProperties []property.Property
+
+	// First load existing properties from the CSV. We want to preserve these.
+	if csvPropertiesJSON, ok := csv.Annotations["olm.properties"]; ok {
+		var csvProperties []property.Property
+		if err := json.Unmarshal([]byte(csvPropertiesJSON), &csvProperties); err != nil {
+			return fmt.Errorf("failed to unmarshal csv.metadata.annotations['olm.properties']: %w", err)
+		}
+		allProperties = append(allProperties, csvProperties...)
+	}
+
+	// Next, load properties from the metadata/properties.yaml file, if it exists.
+	metadataPropertiesJSON, err := fs.ReadFile(fsys, filepath.Join("metadata", "properties.yaml"))
+	if err != nil && !errors.Is(err, fs.ErrNotExist) {
+		return fmt.Errorf("failed to read properties.yaml file: %w", err)
+	}
+
+	// If there are no properties, we can stick with whatever
+	// was already present in the CSV annotations.
+	if len(metadataPropertiesJSON) == 0 {
+		return nil
+	}
+
+	// Otherwise, we need to parse the properties.yaml file and
+	// append its properties into the CSV annotation.
+	type registryV1Properties struct {
+		Properties []property.Property `json:"properties"`
+	}
+
+	var metadataProperties registryV1Properties
+	if err := yaml.Unmarshal(metadataPropertiesJSON, &metadataProperties); err != nil {
+		return fmt.Errorf("failed to unmarshal metadata/properties.yaml: %w", err)
+	}
+	allProperties = append(allProperties, metadataProperties.Properties...)
+
+	// Lastly re-marshal all the properties back into a JSON array and update the CSV annotation
+	allPropertiesJSON, err := json.Marshal(allProperties)
+	if err != nil {
+		return fmt.Errorf("failed to marshal registry+v1 properties to json: %w", err)
+	}
+	csv.Annotations["olm.properties"] = string(allPropertiesJSON)
+	return nil
+}
+
 func toChart(in RegistryV1, installNamespace string, watchNamespaces []string) (*chart.Chart, error) {
 	plain, err := Convert(in, installNamespace, watchNamespaces)
 	if err != nil {
diff --git a/internal/rukpak/convert/registryv1_test.go b/internal/rukpak/convert/registryv1_test.go
index 8e9171dec..0be7e9e84 100644
--- a/internal/rukpak/convert/registryv1_test.go
+++ b/internal/rukpak/convert/registryv1_test.go
@@ -1,7 +1,9 @@
 package convert
 
 import (
+	"context"
 	"fmt"
+	"os"
 	"strings"
 	"testing"
 
@@ -24,7 +26,7 @@ import (
 
 func TestRegistryV1Converter(t *testing.T) {
 	RegisterFailHandler(Fail)
-	RunSpecs(t, "RegstryV1 suite")
+	RunSpecs(t, "RegistryV1 suite")
 }
 
 var _ = Describe("RegistryV1 Suite", func() {
@@ -418,6 +420,17 @@ var _ = Describe("RegistryV1 Suite", func() {
 			})
 		})
 
+		Context("Should read the registry+v1 bundle filesystem correctly", func() {
+			It("should include metadata/properties.yaml and csv.metadata.annotations['olm.properties'] in chart metadata", func() {
+				fsys := os.DirFS("testdata/combine-properties-bundle")
+				chrt, err := RegistryV1ToHelmChart(context.Background(), fsys, "", nil)
+				Expect(err).NotTo(HaveOccurred())
+				Expect(chrt).NotTo(BeNil())
+				Expect(chrt.Metadata).NotTo(BeNil())
+				Expect(chrt.Metadata.Annotations).To(HaveKeyWithValue("olm.properties", `[{"type":"from-csv-annotations-key","value":"from-csv-annotations-value"},{"type":"from-file-key","value":"from-file-value"}]`))
+			})
+		})
+
 		Context("Should enforce limitations", func() {
 			It("should not allow bundles with webhooks", func() {
 				By("creating a registry v1 bundle")
diff --git a/internal/rukpak/convert/testdata/combine-properties-bundle/manifests/csv.yaml b/internal/rukpak/convert/testdata/combine-properties-bundle/manifests/csv.yaml
new file mode 100644
index 000000000..a2a620439
--- /dev/null
+++ b/internal/rukpak/convert/testdata/combine-properties-bundle/manifests/csv.yaml
@@ -0,0 +1,10 @@
+apiVersion: operators.operatorframework.io/v1alpha1
+kind: ClusterServiceVersion
+metadata:
+  name: test.v1.0.0
+  annotations:
+    olm.properties: '[{"type":"from-csv-annotations-key", "value":"from-csv-annotations-value"}]'
+spec:
+  installModes:
+    - type: AllNamespaces
+      supported: true
diff --git a/internal/rukpak/convert/testdata/combine-properties-bundle/metadata/annotations.yaml b/internal/rukpak/convert/testdata/combine-properties-bundle/metadata/annotations.yaml
new file mode 100644
index 000000000..e75867f85
--- /dev/null
+++ b/internal/rukpak/convert/testdata/combine-properties-bundle/metadata/annotations.yaml
@@ -0,0 +1,3 @@
+annotations:
+  operators.operatorframework.io.bundle.mediatype.v1: registry+v1
+  operators.operatorframework.io.bundle.package.v1: test
diff --git a/internal/rukpak/convert/testdata/combine-properties-bundle/metadata/properties.yaml b/internal/rukpak/convert/testdata/combine-properties-bundle/metadata/properties.yaml
new file mode 100644
index 000000000..1a6e7abfb
--- /dev/null
+++ b/internal/rukpak/convert/testdata/combine-properties-bundle/metadata/properties.yaml
@@ -0,0 +1,3 @@
+properties:
+  - type: "from-file-key"
+    value: "from-file-value"