diff --git a/devtools/client/inspector/rules/models/element-style.js b/devtools/client/inspector/rules/models/element-style.js
index 9d9fdc871945..fd700bc94064 100644
--- a/devtools/client/inspector/rules/models/element-style.js
+++ b/devtools/client/inspector/rules/models/element-style.js
@@ -62,6 +62,7 @@ class ElementStyle {
     this.rules = [];
     this.cssProperties = this.ruleView.cssProperties;
     this.variablesMap = new Map();
+    this.startingStyleVariablesMap = new Map();
 
     // We don't want to overwrite this.store.userProperties so we only create it
     // if it doesn't already exist.
@@ -306,6 +307,9 @@ class ElementStyle {
 
     // CSS Variables inherits from the normal element in case of pseudo element.
     const variables = new Map(pseudo ? this.variablesMap.get("") : null);
+    const startingStyleVariables = new Map(
+      pseudo ? this.startingStyleVariablesMap.get("") : null
+    );
 
     // Walk over the computed properties. As we see a property name
     // for the first time, mark that property's name as taken by this
@@ -377,6 +381,10 @@ class ElementStyle {
           earlierInStartingStyle._overriddenDirty =
             !earlierInStartingStyle._overriddenDirty;
           earlierInStartingStyle.overridden = true;
+          // which means we also need to remove the variable from startingStyleVariables
+          if (isCssVariable(computedProp.name)) {
+            startingStyleVariables.delete(computedProp.name);
+          }
         }
 
         // This computed property is overridden if:
@@ -407,12 +415,13 @@ class ElementStyle {
           // get the initial value from the registered property definition.
           if (
             isCssVariable(computedProp.name) &&
-            !computedProp.textProp.invisible &&
-            // variables set in starting-style rules should only impact the starting style
-            // value, not the "final" one.
-            !isPropInStartingStyle
+            !computedProp.textProp.invisible
           ) {
-            variables.set(computedProp.name, computedProp.value);
+            if (!isPropInStartingStyle) {
+              variables.set(computedProp.name, computedProp.value);
+            } else {
+              startingStyleVariables.set(computedProp.name, computedProp.value);
+            }
           }
         }
       }
@@ -425,8 +434,17 @@ class ElementStyle {
         k => variables.get(k) !== previousVariablesMap.get(k)
       )
     );
+    const previousStartingStyleVariablesMap = new Map(
+      this.startingStyleVariablesMap.get(pseudo)
+    );
+    const changedStartingStyleVariableNamesSet = new Set(
+      [...variables.keys(), ...previousStartingStyleVariablesMap.keys()].filter(
+        k => variables.get(k) !== previousStartingStyleVariablesMap.get(k)
+      )
+    );
 
     this.variablesMap.set(pseudo, variables);
+    this.startingStyleVariablesMap.set(pseudo, startingStyleVariables);
 
     // For each TextProperty, mark it overridden if all of its computed
     // properties are marked overridden. Update the text property's associated
@@ -440,7 +458,11 @@ class ElementStyle {
       // of the updated CSS variable names.
       if (
         this._updatePropertyOverridden(textProp) ||
-        this._hasUpdatedCSSVariable(textProp, changedVariableNamesSet)
+        this._hasUpdatedCSSVariable(textProp, changedVariableNamesSet) ||
+        this._hasUpdatedCSSVariable(
+          textProp,
+          changedStartingStyleVariableNamesSet
+        )
       ) {
         textProp.updateEditor();
       }
@@ -912,6 +934,7 @@ class ElementStyle {
    */
   getVariableData(name, pseudo = "") {
     const variables = this.variablesMap.get(pseudo);
+    const startingStyleVariables = this.startingStyleVariablesMap.get(pseudo);
     const registeredPropertiesMap =
       this.ruleView.getRegisteredPropertiesForSelectedNodeTarget();
 
@@ -921,6 +944,9 @@ class ElementStyle {
       // Will be handled in Bug 1866712
       data.value = variables.get(name);
     }
+    if (startingStyleVariables?.has(name)) {
+      data.startingStyle = startingStyleVariables.get(name);
+    }
     if (registeredPropertiesMap?.has(name)) {
       data.registeredProperty = registeredPropertiesMap.get(name);
     }
@@ -939,26 +965,51 @@ class ElementStyle {
    */
   getAllCustomProperties(pseudo = "") {
     let customProperties = this.variablesMap.get(pseudo);
+    const startingStyleCustomProperties =
+      this.startingStyleVariablesMap.get(pseudo);
 
     const registeredPropertiesMap =
       this.ruleView.getRegisteredPropertiesForSelectedNodeTarget();
 
-    // If there's no registered properties, we can return the Map as is
-    if (!registeredPropertiesMap || registeredPropertiesMap.size === 0) {
+    // If there's no registered properties nor starting style ones, we can return the Map as is
+    if (
+      (!registeredPropertiesMap || registeredPropertiesMap.size === 0) &&
+      (!startingStyleCustomProperties ||
+        startingStyleCustomProperties.size === 0)
+    ) {
       return customProperties;
     }
 
     let newMapCreated = false;
-    for (const [name, propertyDefinition] of registeredPropertiesMap) {
-      // Only set the registered property if it's not defined (i.e. not in this.variablesMap)
-      if (!customProperties.has(name)) {
-        // Since we want to return registered property, we need to create a new Map
-        // to not modify the one in this.variablesMap.
-        if (!newMapCreated) {
-          customProperties = new Map(customProperties);
-          newMapCreated = true;
+
+    if (startingStyleCustomProperties) {
+      for (const [name, value] of startingStyleCustomProperties) {
+        // Only set the starting style property if it's not defined (i.e. not in the "main"
+        // variable map)
+        if (!customProperties.has(name)) {
+          // Since we want to return starting style variables, we need to create a new Map
+          // to not modify the one in the main map.
+          if (!newMapCreated) {
+            customProperties = new Map(customProperties);
+            newMapCreated = true;
+          }
+          customProperties.set(name, value);
+        }
+      }
+    }
+
+    if (registeredPropertiesMap) {
+      for (const [name, propertyDefinition] of registeredPropertiesMap) {
+        // Only set the registered property if it's not defined (i.e. not in the variable map)
+        if (!customProperties.has(name)) {
+          // Since we want to return registered property, we need to create a new Map
+          // to not modify the one in the variable map.
+          if (!newMapCreated) {
+            customProperties = new Map(customProperties);
+            newMapCreated = true;
+          }
+          customProperties.set(name, propertyDefinition.initialValue);
         }
-        customProperties.set(name, propertyDefinition.initialValue);
       }
     }
 
diff --git a/devtools/client/inspector/rules/test/browser_rules_at_starting-style.js b/devtools/client/inspector/rules/test/browser_rules_at_starting-style.js
index e415ec3d92a2..fb3fc3177097 100644
--- a/devtools/client/inspector/rules/test/browser_rules_at_starting-style.js
+++ b/devtools/client/inspector/rules/test/browser_rules_at_starting-style.js
@@ -7,6 +7,18 @@
 
 const TEST_URI = `
   <style>
+    @property --my-registered-color {
+      syntax: "<color>";
+      inherits: true;
+      initial-value: blue;
+    }
+
+    @property --my-unset-registered-color {
+      syntax: "<color>";
+      inherits: true;
+      initial-value: lavender;
+    }
+
     h1, [data-test="top-level"] {
       color: tomato;
       transition: all 1s;
@@ -33,6 +45,12 @@ const TEST_URI = `
 
       main, [data-test="in-starting-style"] {
         --my-color: black !important;
+        --my-overridden-color: black;
+        --my-registered-color: black !important;
+        --check-my-color: var(--my-color);
+        --check-my-overridden-color: var(--my-overridden-color);
+        --check-my-registered-color: var(--my-registered-color);
+        --check-my-unset-registered-color: var(--my-unset-registered-color);
         background-color: dodgerblue;
         padding-top: 1px;
         margin-top: 1px !important;
@@ -60,6 +78,10 @@ const TEST_URI = `
 
     main, [data-test="top-level"] {
       --my-color: white;
+      --my-overridden-color: white !important;
+      --my-registered-color: white;
+      --check-my-overridden-color: var(--my-overridden-color);
+      --check-my-registered-color: var(--my-registered-color);
       color: var(--my-color);
       background-color: firebrick;
       padding-top: 2px !important;
@@ -244,21 +266,126 @@ add_task(async function () {
     !isPropertyOverridden(view, 2, { "--my-color": "white" }),
     "--my-color value in top level rule is not overridden"
   );
-  const variableEl = getRuleViewProperty(
+
+  info(
+    "Check var() in regular rule for a variable set in both regular and starting-style rule"
+  );
+  await assertVariableTooltipForProperty(
     view,
     `main, [data-test="top-level"]`,
-    "color"
-  ).valueSpan.querySelector(".ruleview-variable");
-  is(
-    variableEl.dataset.variable,
-    "--my-color = white",
-    "variable popup for --my-color has the expected value"
+    "color",
+    {
+      header: "--my-color = white",
+      // The starting-style value is displayed in the tooltip
+      startingStyle: "--my-color = black",
+    }
+  );
+
+  info(
+    "Check var() in starting-style rule for a variable set in both regular and starting-style rule"
+  );
+  await assertVariableTooltipForProperty(
+    view,
+    `main, [data-test="in-starting-style"]`,
+    "--check-my-color",
+    {
+      // The displayed value is the one set in the starting-style rule
+      header: "--my-color = black",
+      // The starting-style section is not displayed when hovering starting-style rule
+      startingStyle: null,
+    }
+  );
+
+  info(
+    "Check var() in both regular and starting-style rule for a variable overridden in regular rule"
+  );
+  ok(
+    isPropertyOverridden(view, 3, { "--my-overridden-color": "black" }),
+    "--my-overridden-color in top-level starting style rule is overridden"
+  );
+  await assertVariableTooltipForProperty(
+    view,
+    `main, [data-test="top-level"]`,
+    "--check-my-overridden-color",
+    {
+      header: "--my-overridden-color = white",
+      // The starting-style rule is overridden, so we don't show a starting-style section in the tooltip
+      startingStyle: null,
+    }
+  );
+  await assertVariableTooltipForProperty(
+    view,
+    `main, [data-test="in-starting-style"]`,
+    "--check-my-overridden-color",
+    {
+      // the value is the one from the regular rule, not the one from the starting-style rule
+      header: "--my-overridden-color = white",
+      startingStyle: null,
+    }
+  );
+
+  info(
+    "Check var() for a registered property in both regular and starting-style rule"
+  );
+  await assertVariableTooltipForProperty(
+    view,
+    `main, [data-test="top-level"]`,
+    "--check-my-registered-color",
+    {
+      header: "--my-registered-color = white",
+      // The starting-style value is displayed in the tooltip
+      startingStyle: "--my-registered-color = black",
+      // registered property data is displayed
+      registeredProperty: [
+        `syntax:"<color>"`,
+        `inherits:true`,
+        `initial-value:blue`,
+      ],
+    }
+  );
+
+  await assertVariableTooltipForProperty(
+    view,
+    `main, [data-test="in-starting-style"]`,
+    "--check-my-registered-color",
+    {
+      // The displayed value is the one set in the starting-style rule
+      header: "--my-registered-color = black",
+      // The starting-style section is not displayed when hovering starting-style rule
+      startingStyle: null,
+      // registered property data is displayed
+      registeredProperty: [
+        `syntax:"<color>"`,
+        `inherits:true`,
+        `initial-value:blue`,
+      ],
+    }
+  );
+
+  info("Check var() for a unset registered property in starting-style rule");
+  await assertVariableTooltipForProperty(
+    view,
+    `main, [data-test="in-starting-style"]`,
+    "--check-my-unset-registered-color",
+    {
+      // The displayed value is the registered property initial value
+      header: "--my-unset-registered-color = lavender",
+      // The starting-style section is not displayed when hovering starting-style rule
+      startingStyle: null,
+      // registered property data is displayed
+      registeredProperty: [
+        `syntax:"<color>"`,
+        `inherits:true`,
+        `initial-value:lavender`,
+      ],
+    }
   );
 
   async function assertRules(nodeSelector, expectedRules) {
     await selectNode(nodeSelector, inspector);
     const rulesInView = Array.from(
-      view.element.querySelectorAll(".ruleview-rule")
+      // don't retrieve @property rules
+      view.element.querySelectorAll(".ruleview-rule:not([data-name])")
     );
     is(
       rulesInView.length,
diff --git a/devtools/client/inspector/rules/test/browser_rules_registered-custom-properties.js b/devtools/client/inspector/rules/test/browser_rules_registered-custom-properties.js
index fb517c4e6b67..9cec84aefead 100644
--- a/devtools/client/inspector/rules/test/browser_rules_registered-custom-properties.js
+++ b/devtools/client/inspector/rules/test/browser_rules_registered-custom-properties.js
@@ -148,61 +148,61 @@ add_task(async function () {
   checkRegisteredProperties(view, expectedProperties);
 
   info("Check that var() tooltips handle registered properties");
-  await checkVariableTooltipForProperty(
-    view,
-    "h1",
-    "background-color",
+  await assertVariableTooltipForProperty(view, "h1", "background-color", {
     // The variable value is the initial value since the variable does not inherit
-    `--css-no-inherit = ${CSS_NO_INHERIT_INITIAL_VALUE}`,
-    [
+    header: `--css-no-inherit = ${CSS_NO_INHERIT_INITIAL_VALUE}`,
+    registeredProperty: [
       `syntax:"<color>"`,
       `inherits:false`,
       `initial-value:${CSS_NO_INHERIT_INITIAL_VALUE}`,
-    ]
-  );
-  await checkVariableTooltipForProperty(
-    view,
-    "h1",
-    "color",
+    ],
+  });
+  await assertVariableTooltipForProperty(view, "h1", "color", {
     // The variable value is the value set in the main selector, since the variable does inherit
-    `--css-inherit = ${CSS_INHERIT_MAIN_VALUE}`,
-    [
+    header: `--css-inherit = ${CSS_INHERIT_MAIN_VALUE}`,
+    registeredProperty: [
       `syntax:"<color>"`,
       `inherits:true`,
       `initial-value:${CSS_INHERIT_INITIAL_VALUE}`,
-    ]
-  );
-  await checkVariableTooltipForProperty(
+    ],
+  });
+  await assertVariableTooltipForProperty(
     view,
     "h1",
     "border-color",
     // The variable value is the initial value since the variable is not set
-    `--css-not-defined = ${CSS_NOT_DEFINED_INITIAL_VALUE}`,
-    [
-      `syntax:"<color>"`,
-      `inherits:true`,
-      `initial-value:${CSS_NOT_DEFINED_INITIAL_VALUE}`,
-    ]
+    {
+      header: `--css-not-defined = ${CSS_NOT_DEFINED_INITIAL_VALUE}`,
+      registeredProperty: [
+        `syntax:"<color>"`,
+        `inherits:true`,
+        `initial-value:${CSS_NOT_DEFINED_INITIAL_VALUE}`,
+      ],
+    }
   );
-  await checkVariableTooltipForProperty(
+  await assertVariableTooltipForProperty(
     view,
     "h1",
     "height",
     // The variable value is the initial value since the variable does not inherit
-    `--js-no-inherit = ${JS_NO_INHERIT_INITIAL_VALUE}`,
-    [
-      `syntax:"<length>"`,
-      `inherits:false`,
-      `initial-value:${JS_NO_INHERIT_INITIAL_VALUE}`,
-    ]
+    {
+      header: `--js-no-inherit = ${JS_NO_INHERIT_INITIAL_VALUE}`,
+      registeredProperty: [
+        `syntax:"<length>"`,
+        `inherits:false`,
+        `initial-value:${JS_NO_INHERIT_INITIAL_VALUE}`,
+      ],
+    }
   );
-  await checkVariableTooltipForProperty(
+  await assertVariableTooltipForProperty(
     view,
     "h1",
     "width",
     // The variable value is the value set in the main selector, since the variable does inherit
-    `--js-inherit = ${JS_INHERIT_MAIN_VALUE}`,
-    [`syntax:"*"`, `inherits:true`]
+    {
+      header: `--js-inherit = ${JS_INHERIT_MAIN_VALUE}`,
+      registeredProperty: [`syntax:"*"`, `inherits:true`],
+    }
   );
 
   info(
@@ -241,13 +241,14 @@ add_task(async function () {
   );
 
   // The var() tooltip should show the initial value of the new property
-  await checkVariableTooltipForProperty(
-    view,
-    "h1",
-    "caret-color",
-    `--css-dynamic-registered = orchid`,
-    [`syntax:"<color>"`, `inherits:false`, `initial-value:orchid`]
-  );
+  await assertVariableTooltipForProperty(view, "h1", "caret-color", {
+    header: `--css-dynamic-registered = orchid`,
+    registeredProperty: [
+      `syntax:"<color>"`,
+      `inherits:false`,
+      `initial-value:orchid`,
+    ],
+  });
 
   info("Check that updating property does update rules view");
   onRuleViewRefreshed = view.once("ruleview-refreshed");
@@ -281,13 +282,14 @@ add_task(async function () {
   );
 
   // The var() tooltip should show the new initial value of the updated property
-  await checkVariableTooltipForProperty(
-    view,
-    "h1",
-    "caret-color",
-    `--css-dynamic-registered = purple`,
-    [`syntax:"<color>"`, `inherits:true`, `initial-value:purple`]
-  );
+  await assertVariableTooltipForProperty(view, "h1", "caret-color", {
+    header: `--css-dynamic-registered = purple`,
+    registeredProperty: [
+      `syntax:"<color>"`,
+      `inherits:true`,
+      `initial-value:purple`,
+    ],
+  });
 
   info("Check that removing property does update rules view");
   await SpecialPowers.spawn(gBrowser.selectedBrowser, [], () => {
@@ -304,12 +306,9 @@ add_task(async function () {
   checkRegisteredProperties(view, expectedProperties);
 
   // The var() tooltip should indicate that the property isn't set anymore
-  await checkVariableTooltipForProperty(
-    view,
-    "h1",
-    "caret-color",
-    `--css-dynamic-registered is not set`
-  );
+  await assertVariableTooltipForProperty(view, "h1", "caret-color", {
+    header: `--css-dynamic-registered is not set`,
+  });
 
   info(
     "Check that registered properties from new constructed stylesheets are displayed"
@@ -353,13 +352,14 @@ add_task(async function () {
   );
 
   // The `var()` tooltip should show the initial-value of the new property
-  await checkVariableTooltipForProperty(
-    view,
-    "h1",
-    "outline",
-    `--constructed = aqua`,
-    [`syntax:"<color>"`, `inherits:true`, `initial-value:aqua`]
-  );
+  await assertVariableTooltipForProperty(view, "h1", "outline", {
+    header: `--constructed = aqua`,
+    registeredProperty: [
+      `syntax:"<color>"`,
+      `inherits:true`,
+      `initial-value:aqua`,
+    ],
+  });
 
   info(
     "Check that selecting a node in another document with no registered property hides the container"
@@ -552,53 +552,3 @@ function checkRegisteredProperties(view, expectedProperties) {
     }
   }
 }
-
-/**
- * Check the content of a `var()` tooltip on a given rule and property name.
- *
- * @param {CssRuleView} view
- * @param {String} ruleSelector
- * @param {String} propertyName
- * @param {String} expectedTooltipValueContent
- * @param {Array<String>} expectedTooltipRegisteredPropertyContent
- */
-async function checkVariableTooltipForProperty(
-  view,
-  ruleSelector,
-  propertyName,
-  expectedTooltipValueContent,
-  expectedTooltipRegisteredPropertyContent
-) {
-  // retrieve tooltip target
-  const variableEl = await waitFor(() =>
-    getRuleViewProperty(
-      view,
-      ruleSelector,
-      propertyName
-    ).valueSpan.querySelector(".ruleview-variable,.ruleview-unmatched-variable")
-  );
-
-  const previewTooltip = await assertShowPreviewTooltip(view, variableEl);
-  const [valueEl, registeredPropertyEl] = previewTooltip.panel.querySelectorAll(
-    ".variable-value,.registered-property"
-  );
-  is(
-    valueEl.textContent,
-    expectedTooltipValueContent,
-    `CSS variable preview tooltip shows the expected value for ${propertyName} in ${ruleSelector}`
-  );
-  if (!expectedTooltipRegisteredPropertyContent) {
-    is(
-      registeredPropertyEl,
-      undefined,
-      `CSS variable preview tooltip doesn't have registered property section for ${propertyName} in ${ruleSelector}`
-    );
-  } else {
-    is(
-      registeredPropertyEl.innerText,
-      expectedTooltipRegisteredPropertyContent.join("\n"),
-      `CSS variable preview tooltip has expected registered property section for ${propertyName} in ${ruleSelector}`
-    );
-  }
-  await assertTooltipHiddenOnMouseOut(previewTooltip, variableEl);
-}
diff --git a/devtools/client/inspector/rules/utils/utils.js b/devtools/client/inspector/rules/utils/utils.js
index 6b776da98a3b..ffce4b6f0f2c 100644
--- a/devtools/client/inspector/rules/utils/utils.js
+++ b/devtools/client/inspector/rules/utils/utils.js
@@ -166,6 +166,7 @@ function getNodeInfo(node, elementStyle) {
       sheetHref: rule.domRule.href,
       textProperty: declaration,
       variable: node.dataset.variable,
+      startingStyleVariable: node.dataset.startingStyleVariable,
       registeredProperty: {
         initialValue: node.dataset.registeredPropertyInitialValue,
         syntax: node.dataset.registeredPropertySyntax,
diff --git a/devtools/client/inspector/rules/views/text-property-editor.js b/devtools/client/inspector/rules/views/text-property-editor.js
index d156606dede6..30a20626ce28 100644
--- a/devtools/client/inspector/rules/views/text-property-editor.js
+++ b/devtools/client/inspector/rules/views/text-property-editor.js
@@ -611,6 +611,7 @@ TextPropertyEditor.prototype = {
           varName,
           this.rule.pseudoElement
         ),
+      inStartingStyleRule: this.rule.isInStartingStyle(),
     };
     const frag = outputParser.parseCssProperty(name, val, parserOptions);
 
diff --git a/devtools/client/inspector/shared/tooltips-overlay.js b/devtools/client/inspector/shared/tooltips-overlay.js
index 0f1ecfcf3738..80e2c431400e 100644
--- a/devtools/client/inspector/shared/tooltips-overlay.js
+++ b/devtools/client/inspector/shared/tooltips-overlay.js
@@ -347,8 +347,13 @@ TooltipsOverlay.prototype = {
       type === TOOLTIP_VARIABLE_TYPE &&
       nodeInfo.value.value.startsWith("--")
     ) {
-      const { variable, registeredProperty } = nodeInfo.value;
-      await this._setVariablePreviewTooltip(variable, registeredProperty);
+      const { variable, registeredProperty, startingStyleVariable } =
+        nodeInfo.value;
+      await this._setVariablePreviewTooltip({
+        topSectionText: variable,
+        registeredProperty,
+        startingStyle: startingStyleVariable,
+      });
 
       this.sendOpenScalarToTelemetry(type);
 
@@ -539,17 +544,16 @@ TooltipsOverlay.prototype = {
   /**
    * Set the content of the preview tooltip to display a variable preview.
    *
-   * @param {String} text
-   *        The text to display for the variable tooltip
+   * @param {Object} tooltipParams
+   *        See VariableTooltipHelper#setVariableTooltip `params`.
    * @return {Promise} A promise that resolves when the preview tooltip content is ready
    */
-  async _setVariablePreviewTooltip(text, registeredProperty) {
+  async _setVariablePreviewTooltip(tooltipParams) {
     const doc = this.view.inspector.panelDoc;
     await setVariableTooltip(
       this.getTooltip("previewTooltip"),
       doc,
-      text,
-      registeredProperty
+      tooltipParams
     );
   },
 
diff --git a/devtools/client/inspector/test/head.js b/devtools/client/inspector/test/head.js
index 73c8902c6b35..1d804dd60457 100644
--- a/devtools/client/inspector/test/head.js
+++ b/devtools/client/inspector/test/head.js
@@ -998,6 +998,82 @@ async function assertTooltipHiddenOnMouseOut(tooltip, target) {
   ok(!tooltip.isVisible(), "The tooltip is hidden on mouseout");
 }
 
+/**
+ * Check the content of a `var()` tooltip on a given rule and property name.
+ *
+ * @param {CssRuleView} view
+ * @param {String} ruleSelector
+ * @param {String} propertyName
+ * @param {Object} tooltipExpected
+ * @param {String} tooltipExpected.header: The text that is displayed in the top section
+ *        (might be the only section when the variable is not a registered property and
+ *        there is no starting-style).
+ * @param {String} tooltipExpected.startingStyle: The text that is displayed in the starting-style
+ *        section. Pass undefined if the tooltip isn't supposed to have a `@starting-style` section.
+ * @param {Array<String>} tooltipExpected.registeredProperty: Array of the registered property
+ *        fields (e.g. [`syntax:"<color>"`, `inherits:true`, `initial-value:aqua`]).
+ *        Pass undefined if the tooltip isn't supposed to have a @property section.
+ */
+async function assertVariableTooltipForProperty(
+  view,
+  ruleSelector,
+  propertyName,
+  { header, registeredProperty, startingStyle }
+) {
+  // retrieve tooltip target
+  const variableEl = await waitFor(() =>
+    getRuleViewProperty(
+      view,
+      ruleSelector,
+      propertyName
+    ).valueSpan.querySelector(".ruleview-variable,.ruleview-unmatched-variable")
+  );
+
+  const previewTooltip = await assertShowPreviewTooltip(view, variableEl);
+  const valueEl = previewTooltip.panel.querySelector(".variable-value");
+  const startingStyleEl = previewTooltip.panel.querySelector(
+    ".starting-style div"
+  );
+  const registeredPropertyEl = previewTooltip.panel.querySelector(
+    ".registered-property dl"
+  );
+  is(
+    valueEl.textContent,
+    header,
+    `CSS variable preview tooltip has expected header text for ${propertyName} in ${ruleSelector}`
+  );
+
+  if (!registeredProperty) {
+    is(
+      registeredPropertyEl,
+      null,
+      `CSS variable preview tooltip doesn't have registered property section for ${propertyName} in ${ruleSelector}`
+    );
+  } else {
+    is(
+      registeredPropertyEl.innerText,
+      registeredProperty.join("\n"),
+      `CSS variable preview tooltip has expected registered property section for ${propertyName} in ${ruleSelector}`
+    );
+  }
+
+  if (!startingStyle) {
+    is(
+      startingStyleEl,
+      null,
+      `CSS variable preview tooltip doesn't have a starting-style section for ${propertyName} in ${ruleSelector}`
+    );
+  } else {
+    is(
+      startingStyleEl.innerText,
+      startingStyle,
+      `CSS variable preview tooltip has expected starting-style section for ${propertyName} in ${ruleSelector}`
+    );
+  }
+
+  await assertTooltipHiddenOnMouseOut(previewTooltip, variableEl);
+}
+
 /**
  * Get the text displayed for a given DOM Element's textContent within the
  * markup view.
diff --git a/devtools/client/shared/output-parser.js b/devtools/client/shared/output-parser.js
index fd844efd3be8..00e525de16ff 100644
--- a/devtools/client/shared/output-parser.js
+++ b/devtools/client/shared/output-parser.js
@@ -297,31 +297,57 @@ class OutputParser {
     const secondOpts = {};
 
     let varData;
-    let varValue;
     let varFallbackValue;
+    let varSubsitutedValue;
 
     // Get the variable value if it is in use.
     if (tokens && tokens.length === 1) {
       varData = options.getVariableData(tokens[0].text);
-      varValue =
+      const varValue =
         typeof varData.value === "string"
           ? varData.value
           : varData.registeredProperty?.initialValue;
+
+      const varStartingStyleValue =
+        typeof varData.startingStyle === "string"
+          ? varData.startingStyle
+          : // If the variable is not set in starting style, then it will default to either:
+            // - a declaration in a "regular" rule
+            // - or if there's no declaration in regular rule, to the registered property initial-value.
+            varValue;
+
+      varSubsitutedValue = options.inStartingStyleRule
+        ? varStartingStyleValue
+        : varValue;
     }
 
     // Get the variable name.
     const varName = text.substring(tokens[0].startOffset, tokens[0].endOffset);
 
-    if (typeof varValue === "string") {
+    if (typeof varSubsitutedValue === "string") {
       // The variable value is valid, set the variable name's title of the first argument
       // in var() to display the variable name and value.
       firstOpts["data-variable"] = STYLE_INSPECTOR_L10N.getFormatStr(
         "rule.variableValue",
         varName,
-        varValue
+        varSubsitutedValue
       );
       firstOpts.class = options.matchedVariableClass;
       secondOpts.class = options.unmatchedVariableClass;
+
+      // Display starting-style value when not in a starting style rule
+      if (
+        !options.inStartingStyleRule &&
+        typeof varData.startingStyle === "string"
+      ) {
+        firstOpts["data-starting-style-variable"] =
+          STYLE_INSPECTOR_L10N.getFormatStr(
+            "rule.variableValue",
+            varName,
+            varData.startingStyle
+          );
+      }
+
       if (varData.registeredProperty) {
         const { initialValue, syntax, inherits } = varData.registeredProperty;
         firstOpts["data-registered-property-initial-value"] = initialValue;
@@ -363,7 +389,7 @@ class OutputParser {
 
     return {
       node: variableNode,
-      value: varValue,
+      value: varSubsitutedValue,
       fallbackValue: varFallbackValue,
     };
   }
@@ -2074,6 +2100,7 @@ class OutputParser {
       baseURI: undefined,
       getVariableData: null,
       unmatchedVariableClass: null,
+      inStartingStyleRule: false,
     };
 
     for (const item in overrides) {
diff --git a/devtools/client/shared/widgets/tooltip/VariableTooltipHelper.js b/devtools/client/shared/widgets/tooltip/VariableTooltipHelper.js
index f1d5ea737984..cb6ae390ec43 100644
--- a/devtools/client/shared/widgets/tooltip/VariableTooltipHelper.js
+++ b/devtools/client/shared/widgets/tooltip/VariableTooltipHelper.js
@@ -14,23 +14,57 @@ const XHTML_NS = "http://www.w3.org/1999/xhtml";
  *         The tooltip instance on which the text preview content should be set.
  * @param  {Document} doc
  *         A document element to create the HTML elements needed for the tooltip.
- * @param  {String} text
- *         Text to display in tooltip.
+ * @param  {Object} params
+ * @param  {String} params.topSectionText
+ *         Text to display in the top section of tooltip (e.g. "--x = blue" or "--x is not defined").
+ * @param  {Object} params.registeredProperty
+ *         Contains the registered property data, if the variable was registered (@property or CSS.registerProperty)
+ * @param  {String} params.registeredProperty.syntax
+ *         The registered property `syntax` value
+ * @param  {Boolean} params.registeredProperty.inherits
+ *         The registered property `inherits` value
+ * @param  {String} params.registeredProperty.initialValue
+ *         The registered property `initial-value`
+ * @param  {String} params.startingStyle
+ *         The text for @starting-style value (e.g. `--x = red`)
  */
-function setVariableTooltip(tooltip, doc, text, registeredProperty) {
+function setVariableTooltip(
+  tooltip,
+  doc,
+  { topSectionText, registeredProperty, startingStyle }
+) {
   // Create tooltip content
   const div = doc.createElementNS(XHTML_NS, "div");
   div.classList.add("devtools-monospace", "devtools-tooltip-css-variable");
 
   const valueEl = doc.createElementNS(XHTML_NS, "section");
   valueEl.classList.add("variable-value");
-  valueEl.append(doc.createTextNode(text));
+  valueEl.append(doc.createTextNode(topSectionText));
   div.appendChild(valueEl);
 
+  // A registered property always have a non-falsy syntax
+  if (typeof startingStyle !== "undefined") {
+    const section = doc.createElementNS(XHTML_NS, "section");
+    section.classList.add("starting-style", "variable-tooltip-section");
+
+    const h2 = doc.createElementNS(XHTML_NS, "h2");
+    h2.append(doc.createTextNode("@starting-style"));
+    const startingStyleValue = doc.createElementNS(XHTML_NS, "div");
+    startingStyleValue.append(doc.createTextNode(startingStyle));
+    section.append(h2, startingStyleValue);
+
+    div.appendChild(section);
+  }
+
   // A registered property always have a non-falsy syntax
   if (registeredProperty?.syntax) {
+    const section = doc.createElementNS(XHTML_NS, "section");
+    section.classList.add("registered-property", "variable-tooltip-section");
+
+    const h2 = doc.createElementNS(XHTML_NS, "h2");
+    h2.append(doc.createTextNode("@property"));
+
     const dl = doc.createElementNS(XHTML_NS, "dl");
-    dl.classList.add("registered-property");
     const addProperty = (label, value, lineBreak = true) => {
       const dt = doc.createElementNS(XHTML_NS, "dt");
       dt.append(doc.createTextNode(label));
@@ -50,7 +84,8 @@ function setVariableTooltip(tooltip, doc, text, registeredProperty) {
       addProperty("initial-value:", registeredProperty.initialValue, false);
     }
 
-    div.appendChild(dl);
+    section.append(h2, dl);
+    div.appendChild(section);
   }
 
   tooltip.panel.innerHTML = "";
diff --git a/devtools/client/themes/tooltips.css b/devtools/client/themes/tooltips.css
index 4af6e3b44047..be623e775e42 100644
--- a/devtools/client/themes/tooltips.css
+++ b/devtools/client/themes/tooltips.css
@@ -94,15 +94,25 @@ strong {
   word-break: break-word;
   max-inline-size: 100vw;
 
-  .variable-value:has(+ .registered-property) {
+  .variable-value:has(+ .variable-tooltip-section) {
     padding-block-end: var(--block-padding);
   }
 
-  .registered-property {
+  .variable-tooltip-section {
     border-block-start: 1px solid var(--theme-splitter-color);
     margin: 0;
-    padding: 0;
-    padding-block-start: var(--block-padding);
+    padding-block: var(--block-padding);
+
+    h2 {
+      margin-block: 0;
+      padding-block-start: 0;
+      padding-block-end: var(--block-padding);
+    }
+
+    dl {
+      padding: 0;
+      margin: 0;
+    }
 
     dt,dd {
       display: inline;