diff --git a/apps/web/src/components/chat/ComposerModelEffort.tsx b/apps/web/src/components/chat/ComposerModelEffort.tsx
index f56997ff2a6a1..f9409e7abf179 100644
--- a/apps/web/src/components/chat/ComposerModelEffort.tsx
+++ b/apps/web/src/components/chat/ComposerModelEffort.tsx
@@ -512,7 +512,7 @@ export function ComposerEffortColumn(props: { traits: TraitsSelectionInput | nul
       </div>
       {/* pt-2.5 puts the first level on the same line as the first model. */}
       <div
-        className="flex min-h-0 flex-1 flex-col gap-0.5 overflow-y-auto overscroll-contain px-2 pt-2.5 pb-1.5"
+        className="flex min-h-0 flex-1 flex-col gap-0.5 overflow-y-auto px-2 pt-2.5 pb-1.5"
         // Capture, so Up and Down on an option row move rows instead of opening its menu.
         onKeyDownCapture={moveBetweenRows}
       >
diff --git a/apps/web/src/components/chat/ModelPickerContent.tsx b/apps/web/src/components/chat/ModelPickerContent.tsx
index 211bbd59dbd98..6a088dcd07e3a 100644
--- a/apps/web/src/components/chat/ModelPickerContent.tsx
+++ b/apps/web/src/components/chat/ModelPickerContent.tsx
@@ -167,6 +167,7 @@ const MODEL_LIST_ESTIMATED_ITEM_SIZE = 32;
 // Rendered heights in `--spacing` units. Chrome is the search box and list padding, plus a 1px border.
 const ROW_UNITS = 8;
 const ROW_SEPARATOR_UNITS = 0.5;
+const LIST_PADDING_UNITS = 5;
 const LIST_CHROME_UNITS = 15.5;
 
 function ModelListSeparator() {
@@ -256,11 +257,13 @@ function ModelPickerList({
   itemKeys,
   extraData,
   renderItem,
+  fitRows,
 }: {
   listRef: RefObject<LegendListRef | null>;
   itemKeys: ReadonlyArray<string>;
   extraData: unknown;
   renderItem: (props: { item: string; index: number }) => ReactNode;
+  fitRows: boolean | undefined;
 }) {
   const [showTopScrollFade, setShowTopScrollFade] = useState(false);
   const [showBottomScrollFade, setShowBottomScrollFade] = useState(false);
@@ -277,7 +280,15 @@ function ModelPickerList({
       className={cn(
         "relative min-h-0 overflow-hidden pr-px",
         itemKeys.length > 0 ? "flex-1" : "h-0",
+        fitRows && "[--row-units:9] sm:[--row-units:8]",
       )}
+      style={
+        fitRows && itemKeys.length > 0
+          ? {
+              flexBasis: `calc(var(--spacing) * (${itemKeys.length} * var(--row-units) + ${(itemKeys.length - 1) * ROW_SEPARATOR_UNITS} + ${LIST_PADDING_UNITS}))`,
+            }
+          : undefined
+      }
     >
       <ComboboxListVirtualized>
         <LegendList<string>
@@ -295,7 +306,8 @@ function ModelPickerList({
           onScroll={updateScrollFades}
           onReady={updateScrollFades}
           className={cn(
-            "scrollbar-gutter-stable h-full overflow-x-hidden overscroll-y-contain py-1.5 [&::-webkit-scrollbar-track]:my-2",
+            "scrollbar-gutter-stable h-full overflow-x-hidden py-1.5 [&::-webkit-scrollbar-track]:my-2",
+            !fitRows && "overscroll-y-contain",
             getVirtualizedScrollFadeClassName({
               top: showTopScrollFade,
               bottom: showBottomScrollFade,
@@ -343,7 +355,7 @@ export const ModelPickerContent = memo(function ModelPickerContent(props: {
   docked?: boolean;
   /** Right at the end of the search text moves into the popup's effort column. */
   onFocusEffort?: () => void;
-  /** Closes the list column, inside the popup's fixed height. */
+  /** Closes the list column. */
   listFooter?: ReactNode;
 }) {
   const {
@@ -436,6 +448,7 @@ export const ModelPickerContent = memo(function ModelPickerContent(props: {
 
   const focusSearchInput = () => {
     searchInputRef.current?.focus({ preventScroll: true });
+    searchInputRef.current?.scrollIntoView({ block: "nearest", inline: "nearest" });
   };
 
   const handleSelectInstance = (instanceId: ProviderInstanceId | "favorites") => {
@@ -817,9 +830,9 @@ export const ModelPickerContent = memo(function ModelPickerContent(props: {
         ref={pickerContentRef}
         className={cn(
           "relative flex w-screen max-w-90 flex-row overflow-hidden",
-          props.docked ? "max-sm:h-56 max-sm:w-full max-sm:max-w-none" : "max-h-86.5",
+          props.docked ? "max-sm:max-h-56 max-sm:w-full max-sm:max-w-none" : "max-h-86.5",
         )}
-        // Docked, the popup sets the height; a minimum here would overflow short windows.
+        // Docked, the list sets the height; a minimum here would overflow short windows.
         style={
           props.docked
             ? undefined
@@ -833,6 +846,7 @@ export const ModelPickerContent = memo(function ModelPickerContent(props: {
       >
         {showSidebar && (
           <ModelPickerSidebar
+            docked={props.docked ?? false}
             selectedInstanceId={selectedInstanceId}
             onSelectInstance={handleSelectInstance}
             onFocusSearch={focusSearchInput}
@@ -893,7 +907,8 @@ export const ModelPickerContent = memo(function ModelPickerContent(props: {
         >
           <div
             className={cn(
-              "flex min-h-0 flex-1 flex-col overflow-hidden bg-muted/40",
+              "flex min-h-0 flex-1 flex-col overflow-hidden",
+              !props.docked && "bg-muted/40",
               showSidebar && "border-l border-border/70",
             )}
           >
@@ -986,6 +1001,7 @@ export const ModelPickerContent = memo(function ModelPickerContent(props: {
             />
 
             <ModelPickerList
+              fitRows={props.docked}
               listRef={modelListRef}
               itemKeys={filteredItemKeys}
               extraData={modelListExtraData}
diff --git a/apps/web/src/components/chat/ModelPickerSidebar.tsx b/apps/web/src/components/chat/ModelPickerSidebar.tsx
index c07b1f33c5fa9..58f0d8d04980a 100644
--- a/apps/web/src/components/chat/ModelPickerSidebar.tsx
+++ b/apps/web/src/components/chat/ModelPickerSidebar.tsx
@@ -35,6 +35,7 @@ export const ModelPickerSidebar = memo(function ModelPickerSidebar(props: {
   onFocusSearch: () => void;
   instanceEntries: ReadonlyArray<ProviderInstanceEntry>;
   showFavorites?: boolean;
+  docked?: boolean;
   disabledInstanceIds?: ReadonlySet<ProviderInstanceId>;
   selectableUnavailableInstanceIds?: ReadonlySet<ProviderInstanceId>;
   getDisabledInstanceTooltip?: (entry: ProviderInstanceEntry) => string;
@@ -69,7 +70,7 @@ export const ModelPickerSidebar = memo(function ModelPickerSidebar(props: {
 
   return (
     <Toolbar.Root
-      className="w-11 shrink-0 overflow-hidden bg-muted/30"
+      className={cn("w-11 shrink-0 overflow-hidden", !props.docked && "bg-muted/30")}
       data-model-picker-sidebar="true"
       aria-label="Providers"
       orientation="vertical"
@@ -82,7 +83,12 @@ export const ModelPickerSidebar = memo(function ModelPickerSidebar(props: {
         }
       }}
     >
-      <div className="h-full overflow-y-auto overscroll-contain [-ms-overflow-style:none] [scrollbar-width:none] [&::-webkit-scrollbar]:hidden">
+      <div
+        className={cn(
+          "h-full overflow-y-auto [-ms-overflow-style:none] [scrollbar-width:none] [&::-webkit-scrollbar]:hidden",
+          !props.docked && "overscroll-contain",
+        )}
+      >
         <div ref={sidebarContentRef} className="relative flex min-h-full flex-col gap-1 p-1">
           {selectedIndicatorTop !== null ? (
             <div
diff --git a/apps/web/src/components/chat/ProviderModelPicker.tsx b/apps/web/src/components/chat/ProviderModelPicker.tsx
index e05736b0d412d..bcd188749337e 100644
--- a/apps/web/src/components/chat/ProviderModelPicker.tsx
+++ b/apps/web/src/components/chat/ProviderModelPicker.tsx
@@ -16,6 +16,7 @@ import {
   useRef,
   useState,
 } from "react";
+import { AnimatedHeight } from "../AnimatedHeight";
 import { Badge } from "../ui/badge";
 import { Popover, PopoverPopup, PopoverTrigger } from "../ui/popover";
 import { Tooltip, TooltipPopup, TooltipTrigger } from "../ui/tooltip";
@@ -308,7 +309,6 @@ export const ProviderModelPicker = memo(function ProviderModelPicker(props: {
         ? {
             docked,
             onFocusEffort: () => void focusEffort("any"),
-            // Inside the fixed height, so switching to or from a ChatGPT plan never resizes it.
             ...(props.selectedModels === undefined
               ? { listFooter: <ChatGptSharingControl provider={activeEntry?.snapshot ?? null} /> }
               : {}),
@@ -457,23 +457,30 @@ export const ProviderModelPicker = memo(function ProviderModelPicker(props: {
         {props.effortColumn ? (
           <DockedPickerContext value={{ modelLabel: triggerTitle }}>
             <div className="flex max-h-(--available-height) flex-col">
-              {/* One fixed height, so a model with more options never resizes the popup. Short
-                  windows shrink it and keep the footer. */}
-              <div className="flex h-86.5 min-h-0 max-sm:h-auto max-sm:flex-col">
-                {picker}
-                <div
-                  data-model-picker-effort
-                  className="flex min-h-0 w-48 flex-col sm:shrink-0 border-l border-border/70 bg-muted/40 max-sm:h-64 max-sm:w-full max-sm:border-t max-sm:border-l-0"
-                  onKeyDown={(event) => {
-                    if (event.key !== "ArrowLeft" || event.altKey || event.ctrlKey || event.metaKey)
-                      return;
-                    event.preventDefault();
-                    event.stopPropagation();
-                    searchInputRef.current?.focus();
-                  }}
-                >
-                  {props.effortColumn}
-                </div>
+              <div className="min-h-0 overflow-y-auto overscroll-y-contain bg-muted/40 [scrollbar-width:none] [&::-webkit-scrollbar]:hidden">
+                <AnimatedHeight>
+                  <div className="flex max-h-86.5 max-sm:max-h-none max-sm:flex-col">
+                    {picker}
+                    <div
+                      data-model-picker-effort
+                      className="flex min-h-0 w-48 flex-col sm:shrink-0 border-l border-border/70 max-sm:max-h-64 max-sm:w-full max-sm:border-t max-sm:border-l-0"
+                      onKeyDown={(event) => {
+                        if (
+                          event.key !== "ArrowLeft" ||
+                          event.altKey ||
+                          event.ctrlKey ||
+                          event.metaKey
+                        )
+                          return;
+                        event.preventDefault();
+                        event.stopPropagation();
+                        searchInputRef.current?.focus();
+                      }}
+                    >
+                      {props.effortColumn}
+                    </div>
+                  </div>
+                </AnimatedHeight>
               </div>
               {props.footer}
             </div>