diff --git a/packages/block-editor/src/hooks/block-fields/index.js b/packages/block-editor/src/hooks/block-fields/index.js
index b086b483d5573c..809e16463fe0e2 100644
--- a/packages/block-editor/src/hooks/block-fields/index.js
+++ b/packages/block-editor/src/hooks/block-fields/index.js
@@ -10,6 +10,7 @@ import {
 import { createHigherOrderComponent } from '@wordpress/compose';
 import { DataForm } from '@wordpress/dataviews';
 import { useContext, useState, useMemo } from '@wordpress/element';
+import { __ } from '@wordpress/i18n';
 
 /**
  * Internal dependencies
@@ -169,7 +170,25 @@ function denormalizeLinkValue( value, fieldDef ) {
 	return result;
 }
 
-function BlockFields( { clientId, blockType, attributes, setAttributes } ) {
+/**
+ * Component that renders a DataForm for a single block's attributes
+ * @param {Object}   props
+ * @param {string}   props.clientId      The clientId of the block.
+ * @param {Object}   props.blockType     The blockType definition.
+ * @param {Object}   props.attributes    The block's attribute values.
+ * @param {Function} props.setAttributes Action to set the block's attributes.
+ * @param {boolean}  props.isCollapsed   Whether the DataForm is rendered as 'collapsed' with only the first field
+ *                                       displayed by default. When collapsed a dropdown is displayed to allow
+ *                                       displaying additional fields. The block's title is displayed as the title.
+ *                                       The collapsed mode is often used when multiple BlockForms are shown together.
+ */
+function BlockFields( {
+	clientId,
+	blockType,
+	attributes,
+	setAttributes,
+	isCollapsed = false,
+} ) {
 	const blockTitle = useBlockDisplayTitle( {
 		clientId,
 		context: 'list-view',
@@ -178,9 +197,19 @@ function BlockFields( { clientId, blockType, attributes, setAttributes } ) {
 
 	const blockTypeFields = blockType?.[ fieldsKey ];
 
-	const [ form, setForm ] = useState( () => {
-		return blockType?.[ formKey ];
-	} );
+	const computedForm = useMemo( () => {
+		if ( ! isCollapsed ) {
+			return blockType?.[ formKey ];
+		}
+
+		// For a collapsed form only show the first field by default.
+		return {
+			...blockType?.[ formKey ],
+			fields: [ blockType?.[ formKey ]?.fields?.[ 0 ] ],
+		};
+	}, [ blockType, isCollapsed ] );
+
+	const [ form, setForm ] = useState( computedForm );
 
 	// Build DataForm fields with proper structure
 	const dataFormFields = useMemo( () => {
@@ -310,21 +339,29 @@ function BlockFields( { clientId, blockType, attributes, setAttributes } ) {
 		<div className="block-editor-block-fields__container">
 			<div className="block-editor-block-fields__header">
 				<HStack spacing={ 1 }>
-					<BlockIcon
-						className="block-editor-block-fields__header-icon"
-						icon={ blockInformation?.icon }
-					/>
-					<Truncate
-						className="block-editor-block-fields__header-title"
-						numberOfLines={ 1 }
-					>
-						{ blockTitle }
-					</Truncate>
-					<FieldsDropdownMenu
-						fields={ dataFormFields }
-						visibleFields={ form.fields }
-						onToggleField={ handleToggleField }
-					/>
+					{ isCollapsed && (
+						<>
+							<BlockIcon
+								className="block-editor-block-fields__header-icon"
+								icon={ blockInformation?.icon }
+							/>
+							<h2 className="block-editor-block-fields__header-title">
+								<Truncate numberOfLines={ 1 }>
+									{ blockTitle }
+								</Truncate>
+							</h2>
+							<FieldsDropdownMenu
+								fields={ dataFormFields }
+								visibleFields={ form.fields }
+								onToggleField={ handleToggleField }
+							/>
+						</>
+					) }
+					{ ! isCollapsed && (
+						<h2 className="block-editor-block-fields__header-title">
+							{ __( 'Content' ) }
+						</h2>
+					) }
 				</HStack>
 			</div>
 			<DataForm
@@ -371,6 +408,7 @@ const withBlockFields = createHigherOrderComponent(
 								<BlockFields
 									{ ...props }
 									blockType={ blockType }
+									isCollapsed
 								/>
 							</PrivateInspectorControlsFill>
 						)
diff --git a/packages/block-editor/src/hooks/block-fields/styles.scss b/packages/block-editor/src/hooks/block-fields/styles.scss
index e4494b67261bc7..83b08d0e881b8d 100644
--- a/packages/block-editor/src/hooks/block-fields/styles.scss
+++ b/packages/block-editor/src/hooks/block-fields/styles.scss
@@ -30,4 +30,6 @@
 
 .block-editor-block-fields__header-title {
 	flex: 1;
+	// Override the default margin on a h2 element.
+	margin: 0 !important;
 }
diff --git a/packages/block-library/src/audio/index.js b/packages/block-library/src/audio/index.js
index d3bb62a3485884..66c7062692cffa 100644
--- a/packages/block-library/src/audio/index.js
+++ b/packages/block-library/src/audio/index.js
@@ -58,7 +58,7 @@ if ( window.__experimentalContentOnlyInspectorFields ) {
 		},
 	];
 	settings[ formKey ] = {
-		fields: [ 'audio' ],
+		fields: [ 'audio', 'caption' ],
 	};
 }
 
diff --git a/packages/block-library/src/button/index.js b/packages/block-library/src/button/index.js
index 846808023c9248..4bdbde757bb6fb 100644
--- a/packages/block-library/src/button/index.js
+++ b/packages/block-library/src/button/index.js
@@ -69,7 +69,7 @@ if ( window.__experimentalContentOnlyInspectorFields ) {
 		},
 	];
 	settings[ formKey ] = {
-		fields: [ 'text' ],
+		fields: [ 'text', 'link' ],
 	};
 }
 
diff --git a/packages/block-library/src/file/index.js b/packages/block-library/src/file/index.js
index 4257495f0c775f..efe0ae979e3ce9 100644
--- a/packages/block-library/src/file/index.js
+++ b/packages/block-library/src/file/index.js
@@ -63,7 +63,7 @@ if ( window.__experimentalContentOnlyInspectorFields ) {
 		},
 	];
 	settings[ formKey ] = {
-		fields: [ 'file' ],
+		fields: [ 'file', 'fileName', 'downloadButtonText' ],
 	};
 }
 
diff --git a/packages/block-library/src/image/index.js b/packages/block-library/src/image/index.js
index fc65703a23c1f7..e8ee1e3404d7d8 100644
--- a/packages/block-library/src/image/index.js
+++ b/packages/block-library/src/image/index.js
@@ -106,7 +106,7 @@ if ( window.__experimentalContentOnlyInspectorFields ) {
 		},
 	];
 	settings[ formKey ] = {
-		fields: [ 'image' ],
+		fields: [ 'image', 'link', 'caption', 'alt' ],
 	};
 }
 
diff --git a/packages/block-library/src/media-text/index.js b/packages/block-library/src/media-text/index.js
index 1de8b84e64f026..d50e6eaaceb1e6 100644
--- a/packages/block-library/src/media-text/index.js
+++ b/packages/block-library/src/media-text/index.js
@@ -83,7 +83,7 @@ if ( window.__experimentalContentOnlyInspectorFields ) {
 		},
 	];
 	settings[ formKey ] = {
-		fields: [ 'media' ],
+		fields: [ 'media', 'link' ],
 	};
 }
 
diff --git a/packages/block-library/src/navigation-link/index.js b/packages/block-library/src/navigation-link/index.js
index a232f54299f593..1a36a0a9526fcb 100644
--- a/packages/block-library/src/navigation-link/index.js
+++ b/packages/block-library/src/navigation-link/index.js
@@ -112,7 +112,7 @@ if ( window.__experimentalContentOnlyInspectorFields ) {
 		},
 	];
 	settings[ formKey ] = {
-		fields: [ 'label' ],
+		fields: [ 'label', 'link' ],
 	};
 }
 
diff --git a/packages/block-library/src/navigation-submenu/index.js b/packages/block-library/src/navigation-submenu/index.js
index 046f959c7223f3..82cf8a6124a3ff 100644
--- a/packages/block-library/src/navigation-submenu/index.js
+++ b/packages/block-library/src/navigation-submenu/index.js
@@ -71,7 +71,7 @@ if ( window.__experimentalContentOnlyInspectorFields ) {
 		},
 	];
 	settings[ formKey ] = {
-		fields: [ 'label' ],
+		fields: [ 'label', 'link' ],
 	};
 }
 
diff --git a/packages/block-library/src/pullquote/index.js b/packages/block-library/src/pullquote/index.js
index 764946b3fc20a2..bd6bcf7cc3dc99 100644
--- a/packages/block-library/src/pullquote/index.js
+++ b/packages/block-library/src/pullquote/index.js
@@ -54,7 +54,7 @@ if ( window.__experimentalContentOnlyInspectorFields ) {
 		},
 	];
 	settings[ formKey ] = {
-		fields: [ 'value' ],
+		fields: [ 'value', 'citation' ],
 	};
 }
 
diff --git a/packages/block-library/src/search/index.js b/packages/block-library/src/search/index.js
index 983f1706a21625..265f2bb119d8df 100644
--- a/packages/block-library/src/search/index.js
+++ b/packages/block-library/src/search/index.js
@@ -50,7 +50,7 @@ if ( window.__experimentalContentOnlyInspectorFields ) {
 		},
 	];
 	settings[ formKey ] = {
-		fields: [ 'label' ],
+		fields: [ 'label', 'buttonText', 'placeholder' ],
 	};
 }
 
diff --git a/packages/block-library/src/social-link/index.js b/packages/block-library/src/social-link/index.js
index 67e98a10b64669..250191d91c7cef 100644
--- a/packages/block-library/src/social-link/index.js
+++ b/packages/block-library/src/social-link/index.js
@@ -44,7 +44,7 @@ if ( window.__experimentalContentOnlyInspectorFields ) {
 		},
 	];
 	settings[ formKey ] = {
-		fields: [ 'link' ],
+		fields: [ 'link', 'label' ],
 	};
 }
 
diff --git a/packages/block-library/src/video/index.js b/packages/block-library/src/video/index.js
index 3a275c91eaca37..37a1907086d53e 100644
--- a/packages/block-library/src/video/index.js
+++ b/packages/block-library/src/video/index.js
@@ -61,7 +61,7 @@ if ( window.__experimentalContentOnlyInspectorFields ) {
 		},
 	];
 	settings[ formKey ] = {
-		fields: [ 'video' ],
+		fields: [ 'video', 'caption' ],
 	};
 }